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Review Tansley review ?April 0 Tansley ??? Tansley ?? 2008 review review Blackwell Oxford, New NPH © 1469-8137 0028-646X ThePhytologist Authors UK Publishing (2008).Ltd Journal compilation © New Phytologist (2008) Tansley review Branching out in new directions: the control of root architecture by lateral root formation Author for correspondence: J. C. Coates Tel: +44 121 414 5478 Fax: +44 121 414 5925 Email: [email protected] C. Nibau*, D. J. Gibbs* and J. C. Coates School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK Received: 21 December 2007 Accepted: 14 March 2008 Contents Summary 595 I. Background 595 II. Formation of lateral roots 596 III. Endogenous factors regulating the stages of lateral root development V. Transcriptomic studies to identify potential new regulators of lateral root development VI. Conclusions and future challenges IV. Plasticity: modification of lateral root development by the environment 597 608 608 Acknowledgements 608 References 609 603 Summary Key words: abiotic stress, biotic stress, lateral root development, nutrients, plant hormones, root system architecture, transcriptomics. Plant roots are required for the acquisition of water and nutrients, for responses to abiotic and biotic signals in the soil, and to anchor the plant in the ground. Controlling plant root architecture is a fundamental part of plant development and evolution, enabling a plant to respond to changing environmental conditions and allowing plants to survive in different ecological niches. Variations in the size, shape and surface area of plant root systems are brought about largely by variations in root branching. Much is known about how root branching is controlled both by intracellular signalling pathays and by environmental signals. Here, we will review this knowledge, with particular emphasis on recent advances in the field that open new and exciting areas of research. New Phytologist (2008) 179: 595–614 © The Authors (2008). Journal compilation © New Phytologist (2008) doi: 10.1111/j.1469-8137.2008.02472.x I. Background A plant’s root system is the site of water and nutrient uptake from the soil, a sensor of abiotic and biotic stresses, and a *These authors contributed equally to this work. www.newphytologist.org structural anchor to support the shoot. The root system communicates with the shoot, and the shoot in turn sends signals to the roots. A plant root system initially consists of a primary root (PR) formed during embryogenesis that has dividing cells in a meristem at its tip. As the seedling develops, certain other cells within the PR acquire the capability to 595 596 Review Tansley review Fig. 1 Components of the root system. (a) A typical dicot (e.g. Arabidopsis) seedling root system, consisting of a primary root (PR) originating from the embryo, lateral roots (LR) branching out from the PR during seedling development, and root hairs (RH) that originate from PR epidermal (Epi) cells (shown at higher magnification to the right (inset)). Ultimately, the LRs will undergo higher-order branching to form secondary and tertiary LRs. Adventitious roots (AR) form at the shoot–root junction. (b) A typical cereal (e.g. rice, maize) seedling root system consisting of a primary root (PR) originating from the embryo, seminal roots (SR) that originate postembryonically close to the top of the primary root, and crown roots (CR) that originate from the stem. PR, SR and CR all form LR and undergo higher-order branching. divide, eventually forming new roots, called lateral roots (LRs) (Fig. 1a). These branch out from the PR, greatly increasing the total surface area and mechanical strength of the root system and allow the plant to explore the soil environment. Ultimately, millions of higher-order root branches can form, resulting in hundreds of miles of root system in a small area of soil (Dittmer, 1937). New roots, called adventitious roots (AR), can also be formed postembryonically at the shoot–root junction, optimizing the exploration of the upper soil layers (Fig. 1a). In cereals such as rice and maize, root structure becomes more complex, with the formation of additional shoot-borne and postembryonic roots, which in turn undergo higher-order branching (Hochholdinger et al., 2004; Hochholdinger & Zimmermann, 2008; Fig. 1b). The root system architecture (RSA) of plants varies hugely between species and also shows extensive natural variation within species, reflecting the plethora of environments in which plants can grow (Cannon, 1949; Loudet et al., 2005; Osmont et al., 2007). Root system architecture manipulation is instrumental in the domestication and breeding of crop plants, because using water and nutrients from the soil in the most efficient manner affects a plant’s ability to survive in stressful or poor soils. Changes in RSA can therefore have huge impacts on the final yield of a crop (reviewed in de Dorlodot et al., 2007). Of the factors that control total RSA, LR formation and growth is one of the most important. Many of the hormonal and environmental signals affecting LR development also affect other components that have a bearing on RSA and the overall root surface area, namely, root New Phytologist (2008) 179: 595–614 hair development, primary root (PR) growth and AR formation. However, an extensive analysis of how these structures are controlled is outside the scope of the present review and the reader is referred to several other excellent reviews (Dolan & Costa, 2001; Carol & Dolan, 2002; Scheres et al., 2002; Casson & Lindsey, 2003; Hochholdinger et al., 2004; Samaj et al., 2004; Serna, 2005; Scheres, 2007). Moreover, colonization of certain plant roots by symbiotic bacteria or fungi leads to the formation of modified LRs (root nodules, mycorrhizas or proteoid roots) that carry out specialized functions such as nutrient acquisition (Oldroyd & Downie, 2004, 2006; Autran et al., 2006). In addition to signals that regulate many components of RSA (and sometimes also shoot development), there is mounting evidence that some signalling networks are specific for LR formation (Rogg et al., 2001; Hochholdinger et al., 2004; Loudet et al., 2005; Coates et al., 2006), potentially highlighting novel strategies for manipulating root branching in crop plants. Because of the major contribution they play in the control of RSA, this review focuses on LRs: how they arise and develop. It will pay particular attention to recent molecular and ‘omic’ developments that highlight the huge variety of genes, proteins and mechanisms that interact together to coordinate a process so central to plant development and survival. II. Formation of lateral roots In flowering plants and gymnosperms, LRs initiate from a specialized cell layer in the PR called the pericycle. The pericycle is the outermost cell layer of the vascular cylinder and consists of two distinct cell types corresponding to the underlying vasculature (Dubrovsky & Rost, 2005; Parizot et al., 2008; Fig. 2a,b). In Arabidopsis and most other dicots, LRs are formed only from pericycle cells overlying the developing xylem tissue (the xylem pole pericycle) (Fig 2b). In other species, particularly cereals such as maize, rice and wheat, LRs arise specifically from the phloem pole pericycle, with additional contributions from the endodermis (De Smet et al., 2006a; Hochholdinger & Zimmermann, 2008; Fig. 2b). Insights into the evolution of multicellular, branched root systems come from ‘ancient’ plants. In a vascular nonseed plant, the fern Ceratopteris, LRs arise from the endodermis and may be regulated differently from those in flowering plants (Hou et al., 2004). The bryophyte moss Physcomitrella patens revealed a very ancient mechanism controlling the development of tissues with a rooting function (Menand et al., 2007). Physcomitrella possesses putative homologues of known Arabidopsis LR regulators, many of which have no assigned function (e.g. Axtell et al., 2007; Rensing et al., 2008). Lateral root formation consists of four key stages: (i) stimulation and dedifferentiation of pericycle founder cells; (ii) cell cycle re-entry and asymmetric cell divisions to give rise to a lateral root primordium (LRP); (iii) LRP emergence through the outer layers of the PR via cell expansion; and (iv) www.newphytologist.org © The Authors (2008). Journal compilation © New Phytologist (2008) Tansley review Review Fig. 2 Root anatomy. (a) Longitudinal section through an Arabidopsis primary root tip, showing the different cell types. LRC, lateral root cap (which is absent further up the root); Epi, epidermis (which is the outermost layer of the root above the root tip); Co, cortex; En, endodermis; P, pericycle; Vasc, vasculature (xylem and phloem); QC, quiescent centre (maintains the neighbouring stem cell population). (b) Transverse section through an Arabidopsis primary root. Epi, epidermis; RH, root hair; Co, cortex; En, endodermis; P, pericycle; XPP, xylem pole pericycle (the pericycle cells adjacent to the xylem tissue, from which lateral roots arise); Xy, xylem; Ph, phloem. In monocots, lateral roots arise from the phloem pole pericycle. Fig. 3 Aspects of auxin signalling during lateral root (LR) development. (a) A pulse of auxin (light grey) in the basal meristem (BM) primes a pericycle cell (dark grey) to become competent to form a lateral root initial cell. (b) Cells (white) leaving the basal meristem between cyclical auxin maxima are not specified to become LR initials. (c) The first primed pericycle cell arrives at a point where it can initiate LR development; meanwhile another pericycle cell (dark grey) is primed in the basal meristem by the subsequent auxin pulse. (d) Lateral root initiation begins with auxin-induced IAA14 degradation. This allows activation of the ARF7 and ARF19 transcription factors, which activate expression of LBD/ ASL genes. LBD/ASL proteins in turn activate cell cycle genes and cell patterning genes, enabling formation of a new lateral root primordium (LRP). Auxin also activates transcription of NAC1 to stimulate LR initiation, and at the same time induces expression of two ubiquitin ligases, CEGUENDO and SINAT5, which feed back to attenuate the auxin response. activation of the LR meristem that recapitulates PR growth (Celenza et al., 1995; Cheng et al., 1995; Laskowski et al., 1995; Malamy & Benfey, 1997). III. Endogenous factors regulating the stages of lateral root development Underpinning each stage of LR development is the hormone auxin (Casimiro et al., 2003; Woodward & Bartel, 2005; Figs 3a–d and 4a–d). Comprehensive studies using a LR- inducible system revealed that over 10% of the Arabidopsis seedling root transcriptome was affected by treatment with auxin (Himanen et al., 2002; Vanneste et al., 2005). Auxin maxima appear at LR initiation sites and also later during emergence and elongation (see section III.1). Auxin ‘hot spots’ within the root arise as a result of the regulated positioning of auxin transporters within cells, in a process conserved between lateral organ formation in the root and in the shoot (Benkova et al., 2003). Interestingly, auxin signalling regulates the differential positioning of auxin efflux carriers © The Authors (2008). Journal compilation © New Phytologist (2008) www.newphytologist.org New Phytologist (2008) 179: 595–614 597 598 Review Tansley review Fig. 4 Lateral root development in Arabidopsis shown in longitudinal section. P, pericycle; En, endodermis; Co, cortex; Epi, epidermis. (a) Early initiation – a founder xylem pole pericycle cell (dark grey) undergoes initial anticlinal cell divisions (perpendicular to the surface of the root). (b) Periclinal cell divisions (parallel to the surface of the root) begin and the lateral root primordium (LRP) begins to grow. (c) The LRP undergoes further organized cell divisions and begins to emerge through the outer cell layers of the primary root, resulting in cell separation (asterisks). (d) The new lateral root is fully emerged and its new meristem is activated (dark grey star). It will continue to grow and elongate. At each stage, the effect of various key plant hormones is indicated. ABA, abscisic acid; BR, brassinosteroids. and, consequently, the direction of auxin flow (Sauer et al., 2006). This effect is mediated by the activity of VPS29, a membrane-trafficking component that is involved in the recycling of cargo molecules. Together with other proteins, VPS29 mediates the dynamic arrangement of auxin efflux carriers in response to auxin (Jaillais et al., 2007). The regulated interplay between auxin transport and signalling is critical for all stages of LR development, and many of the signals regulating RSA impinge upon this pathway. Many Arabidopsis and cereal mutants affecting auxin production, transport and metabolism have LR defects: their involvement in LR formation has been described extensively elsewhere (Casimiro et al., 2003; Woodward & Bartel, 2005; Fukaki et al., 2007). Lack of detailed characterization of many of these mutants prevents identification of the particular stage of LR development at which they act (De Smet et al., 2006a). Exhaustive description of all the proteins involved in auxin-dependent lateral organ formation is beyond the scope of this review and the reader is directed to recent reviews in this area (De Smet et al., 2006a; Teale et al., 2006; De Smet & Jurgens, 2007). Other hormone pathways are also involved in the regulation of LR formation, and recent research provides new insight into these pathways. Below we will outline how plant hormones, with particular emphasis on auxin, interact with various cellular processes to control each stage of LR development. 1. Lateral root initiation – stimulation of cell cycle proliferation in the pericycle In Arabidopsis, the xylem pole pericycle cells, from which LRs arise, are smaller than other pericycle cells, indicating New Phytologist (2008) 179: 595–614 differential cell cycle regulation between pericycle cell types. Normally, not all xylem pole pericycle cells form LRP, indicating that multiple levels of control occur in these cells (Beeckman et al., 2001). However, exogenous application of auxin can activate the whole pericycle to form LRPs, whereas the application of auxin transport inhibitors blocks LR formation without loss of pericycle identity (Casimiro et al., 2001; Himanen et al., 2002). Therefore, all the cells within the pericycle retain the ability to form LRs but only some of them do so. It is thus suggested that the coordinated action of auxin transport and signalling, cell cycle regulators and novel root-specific proteins is necessary for LR initiation to occur. Lateral root initiation requires auxin and regulated protein degradation Auxin signalling during LR initiation is closely coupled with regulated protein degradation (Fig. 3d). Proteins are targeted to the cellular degradation machinery, the proteasome, by the addition of a chain of ubiquitin monomers. The process requires a ubiquitin-activating enzyme (E1), a ubiquitin-conjugating enzyme (E2) and a ubiquitin-protein ligase (E3), which transfers ubiquitin from the E2 to the target (Petroski & Deshaies, 2005). Some E3 ubiquitin ligases consist of multiprotein complexes, and SKP1-CULLIN1-F-box (SCF) E3 ligases contain F-box protein subunits that confer specificity, binding to particular target proteins. Auxin receptors are a family of F-box-containing proteins known as TIR1 and AFB1–3 (Dharmasiri et al., 2005a,b; Kepinski & Leyser, 2005). It is thus not surprising that mutants in components of the SCF complex and its associated proteins have altered LR phenotypes (Gray et al., 1999; Hellmann et al., 2003; Bostick et al., 2004; Chuang et al., 2004; Woodward et al., 2007). www.newphytologist.org © The Authors (2008). Journal compilation © New Phytologist (2008) Tansley review Auxin binding to TIR1/AFBs allows them to interact with AUX/IAA proteins and target them for degradation. AUX/IAA proteins are transcriptional repressors that dimerize with auxin response factor (ARF) transcription factors, preventing the latter from binding to promoter elements in auxinresponsive genes. Thus, auxin-induced degradation of AUX/ IAAs enables ARFs to activate auxin-responsive transcription (Gray et al., 2001; Dharmasiri et al., 2005a,b; Kepinski & Leyser, 2005). AUX/IAAs and ARFs exist as large, functionally redundant protein families (Okushima et al., 2005; Overvoorde et al., 2005). One of the most important AUX/IAA proteins for LR initiation is SLR1/IAA14. As a result of the stabilization of IAA14, a gain-of-function slr1 mutant does not form LRs (Fukaki et al., 2002). In wild-type plants, auxin triggers the degradation of IAA14, enabling ARF7 and ARF19 to activate transcription of LATERAL ORGAN BOUNDARIES DOMAIN/ASYMMETRIC LEAVES LIKE (LBD/ASL) genes (Fukaki et al., 2005; Okushima et al., 2007; and Fig. 3d). LBD/ASL proteins, in turn, activate the transcription of cell proliferation and patterning genes (Okushima et al., 2007). In maize and rice, LBD genes regulate shoot-borne root formation rather than LRs (Taramino et al., 2007; Hochholdinger & Zimmermann, 2008). ARF7 also interacts with a MYB transcription factor that provides a link among auxin, LR initiation and environmental responses (Shin et al., 2007; and section IV.4). Comparison of the auxin-induced transcriptomes of wild-type and slr1 roots identified 913 specific ‘LR initiation’ genes that function downstream of the auxin/slr1 signalling pathway. Many of these are cell cycle-associated genes or cell division-associated genes, and genes involved in auxin signalling, transport or metabolism. Other over-represented functional categories include macromolecular biosynthesis, ribosome biogenesis and DNA synthesis (Vanneste et al., 2005). IAA28 is also important for LR initiation. The gain-offunction mutant iaa28 forms fewer LRs than the wild type: IAA28 is degraded by auxin and represses auxin-induced LR-formation genes. However, IAA28 mRNA levels are repressed by auxin, indicating a complex regulation of IAA28 during auxin signalling (Rogg et al., 2001; Dreher et al., 2006). The iaa28 mutant is also resistant to exogenous cytokinins and ethylene, suggesting an integration point for other hormone pathways. The VIER F-BOX PROTEINE (VFB) F-box proteins are also important for LR formation in Arabidopsis. Mutants deficient in VFB function have reduced LR formation. Microarray analysis demonstrated that loss of VFB function leads to altered expression of both auxin-responsive genes and cell wall-remodelling genes (Schwager et al., 2007). Despite this, vfb mutant plants maintain full sensitivity to exogenously applied auxin. VFBs may regulate auxin-induced gene expression, and consequently LR formation, by a pathway independent of the auxin receptor TIR1 (Schwager et al., Review 2007). It will be important to determine whether IAA14/ SLR1 stability or cell cycle gene expression is affected in vfb mutants. The NAC1 transcription factor promotes LR initiation (Xie et al., 2000) and may bind auxin-responsive promoters to transmit the auxin signal (Fig. 3d). Interestingly, NAC1 overexpression can rescue the reduced LR phenotype of tir1 auxin receptor mutants. NAC1 is tightly regulated: NAC1 expression is induced within 30 min of auxin application, suggesting that NAC1 may be an early auxin-responsive gene. Auxin also induces the expression (albeit more slowly) of SINAT5, a RING-finger ubiquitin E3 ligase (Fig. 3d). SINAT5 promotes NAC1 ubiquitination and subsequent degradation (Xie et al., 2002). It will be interesting to determine if auxin binds directly to SINAT5 in the SINAT5–NAC1 complex. Yet another ubiquitin ligase involved in LR initiation is XBAT32 (Nodzon et al., 2004). XBAT32 is a RING-finger protein highly expressed in the vascular system close to sites of LR initiation. Plants lacking XBAT32 develop fewer LRs than wild-type plants and have reduced cell division in the pericycle. XBAT32 may be involved in auxin transport: loss of XBAT32 may lead to suboptimal auxin levels for LR initiation (Nodzon et al., 2004). As only certain pericycle cells usually give rise to LRs, it is crucial that auxin signals are tightly regulated. Interestingly, auxin stimulates the transcription of ubiquitin ligases that repress auxin signals, providing an elegant feedback mechanism to maintain auxin sensitivity in the pericycle. The F-box protein CEGENDUO (CEG) is a negative regulator of LR formation whose transcription is induced by auxin (Dong et al., 2006; and Fig. 3d). Further studies are needed to clarify its role LR initiation. It is thus clear that the action of auxin during LR initiation depends heavily on the ubiquitin-proteasome pathway, both to transduce signals by degrading repressors and also to reset the system by destroying activators when they are no longer needed. Protein degradation allows for rapid changes in response to the ever-changing environment, as well as providing fine-tuning to sustained signals. Which pericycle cells? Questions remain about where, when and which pericycle cells are primed to become LR initiation sites. In the last year, this problem has been addressed by new molecular genetic and mathematical modelling studies. De Smet et al. (2007) showed that the position of Arabidopsis LR formation is determined in a region at the transition between the meristem and the elongation zone, called the basal meristem (Fig. 3a–c). Lateral roots occurred in a regularly spaced alternating left–right pattern correlating with gravity-induced root waving. Both responses are dependent on the auxin influx transporter, AUX1. Furthermore, auxin responsiveness at the basal meristem oscillates in a periodic manner, correlating with the timing of LR formation. This, together with the observation of a lateral gradient of auxin responsiveness with a maximum in protoxylem © The Authors (2008). Journal compilation © New Phytologist (2008) www.newphytologist.org New Phytologist (2008) 179: 595–614 599 600 Review Tansley review cells, led the authors to suggest that auxin accumulation alone is sufficient for the priming of founder cells (De Smet et al., 2007). Consequently, one can suggest that all the other factors involved in LR formation will act downstream of the auxin signal. However, several factors have been suggested to regulate LR formation independently of auxin (see section III.1 ‘Hormone-independent signalling pathways that regulate lateral root initiation’). Targeted manipulation of these genes in pericycle cells in the basal meristem is necessary to clarify this conundrum. In addition, it is well known that environmental factors can tap into the LR developmental program and alter root architecture in regions outside the basal meristem (see section IV). Support for the co-regulation of LR formation and gravitropism came from a mathematical model suggesting that gravistimulation concentrates auxin at a certain point in the root, allowing the auxin threshold necessary for LR formation to be reached. Lateral root initiation would, in turn, consume the auxin pool in that area, preventing new LR initiation until the pool had been refilled: this would be accelerated by a new gravistimulation (Lucas et al., 2007). Two main ideas came out of this study: first, there is an endogenous mechanism regulating the periodicity of LR formation, revealed by the existence of a minimum and maximum time between two successive LR initiations. Second, this endogenous system is sensitive to external cues such as gravity (Lucas et al., 2007). This would provide increased plasticity for the root system to adapt to new soil conditions. Interestingly, the developmental window for LR initiation in Arabidopsis displays natural variation between accessions (Dubrovsky et al., 2006), which may indicate adaptation of the system to different environmental niches. In addition, LRP initiation and emergence are separable processes, again providing greater plasticity to the root system (Dubrovsky et al., 2006). The mathematical model used by Lucas et al. (2007) suggests that LR formation in gravistimulated areas may also optimize soil exploration. It will be interesting to determine if biotic and abiotic factors that alter RSA also have an effect on gravitropism-stimulated LR formation. It is important to move this type of research beyond Arabidopsis to agriculturally relevant plants, especially as the mechanisms at work in crop plants may differ from those in Arabidopsis. In many grasses, LRs initiate in phloem pole pericycle cells and, because of varying root organization and growth rates, the timing and spacing of LR initiation is also different (Dubrovsky et al., 2006; Dembinsky et al., 2007). Interplay between the cell cycle and auxin signalling It is generally accepted that pericycle cells are arrested in the G1 phase of the cell cycle. Those pericycle cells that will give rise to a LR proceed through S phase and arrest in G2. Lateral root-inducing signals stimulate these cells to undergo proliferative cell divisions (Beeckman et al., 2001). Cell cycle re-entry requires changes in chromatin structure, increasing New Phytologist (2008) 179: 595–614 the proportion of active chromatin in the genome (De Veylder et al., 2007). Indeed, a chromatin remodelling factor mutant has perturbed LR initiation (Fukaki et al., 2006). Cell cycle progression from G1 to S requires the activity of the retinoblastoma (RB)-E2F pathway (del Pozo et al., 2006; De Veylder et al., 2007). Progression from G2 to M is regulated by the opposing activity of B-type cyclin-dependent kinases (CDKs) and CDK inhibitor proteins (KRPs) (Wang et al., 1997; De Veylder et al., 2001; Verkest et al., 2005). Many cell cycle components are transcriptionally regulated by auxin (Himanen et al., 2002; Vanneste et al., 2005). Another level of regulation involves cell cycle protein degradation (Verkest et al., 2005; del Pozo et al., 2006). In tomato, nitric oxide is required in the early stages of LR formation to regulate the expression of cell cycle genes, downstream of the auxin signal (Correa-Aragunde et al., 2006). Nitric oxide is also induced in Arabidopsis LRP by the auxin, indole-3-butyric acid (Kolbert et al., 2007). Despite the importance of the cell cycle in LR initiation, increasing the mitotic index in roots or forcing excessive cell divisions in the pericycle does not stimulate LR initiation or morphogenesis (Vanneste et al., 2005; Wang et al., 2006). Thus, pericycle cell divisions can be uncoupled from LRP formation, and LR initiation seems to require the simultaneous activation of cell cycle and cell fate genes triggered by auxininduced degradation of the SLR/IAA14 protein (Vanneste et al., 2005). Conversely, although cell division and LR morphogenesis are both controlled by auxin signalling, the processes are regulated independently, as shown by tomato diageotropica (dgt) mutants that have a number of auxin-related phenotypes (including a lack of LRs) but have normal root cell identities and patterning. dgt mutant pericycle cells maintain their full proliferative capacity, but no LRs are formed, even in the presence of exogenous auxin, which instead stimulates further pericycle divisions to form multiple cell layers (Ivanchenko et al., 2006). A similar mechanism operates in Arabidopsis, as demonstrated by the wol mutant, which forms very few LRs even in the presence of auxin (Parizot et al., 2008). Close analysis of the pericycle cells in the wol mutant showed that they express pericycle protoxylem markers and are able to divide in response to auxin but no LRPs are formed (Parizot et al., 2008). This again shows that cell cycle activation is not sufficient for LR initiation to occur. Heterotrimeric G-proteins may integrate auxin signalling and cell cycle inputs during root branching as well as other developmental processes (Ullah et al., 2001, 2003; Chen et al., 2006b; Trusov et al., 2007). Mutations in the β or γ G-protein subunits show increased cell division and increased LR formation, and the normal function of Gβ and Gγ may be to attenuate auxin signalling (Ullah et al., 2003; Trusov et al., 2007). Other hormones affecting LR development In addition to auxin, other hormone signals are important for LR initiation (Fig. 4a–d). Traditionally, cytokinin is thought to act www.newphytologist.org © The Authors (2008). Journal compilation © New Phytologist (2008) Tansley review antagonistically to auxin in many developmental processes: indeed, cytokinin is a negative regulator of LR formation in many plant species, including Arabidopsis, Medicago, tobacco and rice (Werner et al., 2003; Rani Debi et al., 2005; Gonzalez-Rizzo et al., 2006; Li et al., 2006b; Laplaze et al., 2007). Plants with decreased cytokinin content have increased LR numbers (Werner et al., 2001, 2003; To et al., 2004; Mason et al., 2005; Gonzalez-Rizzo et al., 2006; Riefler et al., 2006), whereas exogenous cytokinin inhibits LR initiation by preventing pericycle cell cycle re-entry (Li et al., 2006b). An elegant study by Laplaze et al. (2007) showed that exogenous cytokinin disrupts both LR initiation and the organization of cell divisions within developing LRPs: these defects cannot be rescued by auxin. Targeted expression of cytokinin biosynthetic and catabolic enzymes in specific cell types demonstrated that cytokinin activity is required very early in the LR formation process (Laplaze et al., 2007). Importantly, disrupting cytokinin signalling in xylem pole pericycle cells leads to perturbation of the auxin maximum in developing LRPs as a result of the reduced expression of PIN auxin transporter genes and mislocalization of PIN proteins (Laplaze et al., 2007). Both ethylene and brassinosteroids affect LR formation via an auxin-dependent pathway (Bao et al., 2004; Stepanova et al., 2005). In rice, a casein kinase 1 gene, OsCKI, is upregulated by both brassinosteroid and abscisic acid (ABA) and promotes lateral and AR formation as well as cell elongation. OsCKI may affect LR development by regulating endogenous auxin levels (Liu et al., 2003). Transcriptomic analysis of OsCKI-deficient plants revealed alteration of several signalling, developmental, transcriptional and metabolic genes (Liu et al., 2003). Unequivocal evidence for a role of ABA in LR initiation is not available. However, the ABA-insensitive mutant abi3 shows decreased sensitivity to auxin-induced LR initiation (Brady et al., 2003). Furthermore, 9-cis-epoxycarotenoid dioxygenase genes (involved in ABA biosynthesis) are expressed in pericycle cells surrounding LR initiation sites (Tan et al., 2003). It is tempting to suggest that ABA may restrain cell proliferation outside the LR initiation site, although ABA being produced as a result of the stress caused by LR emergence cannot be excluded (De Smet et al., 2006b). Indeed, ABA upregulates the expression of KRP1, a cell cycle inhibitor (Wang et al., 1998). Some auxin-induced LR-initiation genes had previously been described as ABA-repressed (Vanneste et al., 2005). Among these, AUXIN-INDUCED IN ROOT CULTURES 12 (AIR12) and IAA19 function in LR formation (Neuteboom et al., 1999; Tatematsu et al., 2004). Thus, ABA and auxin could have an antagonistic effect on LR initiation (Fig. 4a). Interestingly, the KNAT1 homeobox transcription factor is expressed at the base of LR primordia (Truernit et al., 2006) and is auxin-induced and ABA-repressed in LR primordia (Soucek et al., 2007), suggesting a possible point of integration for the two signals. Further research is needed to establish ABA as an inhibitor of LR initiation in Arabidopsis. Review Curiously, ABA seems to stimulate LR initiation in rice (Chen et al., 2006a). In addition to ‘classical’ plant hormones, several other signals affect LR development both during initiation and at later stages, in a variety of plant species. Salicylic acid promotes LR initiation, emergence and growth, possibly via crosstalk with cytokinin or auxin (Echevarria-Machado et al., 2007). Melatonin promotes lateral and AR formation while decreasing root length, similarly to the effects of auxin (Arnao & Hernandez-Ruiz, 2007). Alkamides are lipid-based secondary metabolites that are novel regulators of plant growth and development (Lopez-Bucio et al., 2006). They induce LR initiation and growth in Arabidopsis (Ramirez-Chavez et al., 2004), and regulate meristematic activity throughout the plant. It is suggested that they regulate root pericycle cell activation, possibly via cytokinin signalling (Lopez-Bucio et al., 2007). Hormone-independent signalling pathways that regulate lateral root initiation The best-characterized protein that regulates LR initiation, independently of hormone signalling, is ABERRANT LATERAL ROOT FORMATION 4 (ALF4). The Arabidopsis alf4 mutant shows a complete absence of LRs, even in the presence of auxin (Celenza et al., 1995). Cells appear to be blocked at a premitotic stage of the cell cycle, but the identity of the xylem pole pericycle itself is not compromised. ALF4 is a nuclear-localized protein of unknown function; a shorter protein generated by alternative splicing localizes to the cytoplasm. Importantly, auxin has no effect on ALF4 levels or intracellular localization (DiDonato et al., 2004). In the current model, ALF4 maintains the pericycle in a ‘competent’ state for cell division, allowing input from other LR-inducing signals, including auxin (DiDonato et al., 2004). The alf4 mutant maintains full responsiveness to auxin inhibition of PR elongation, suggesting that LR formation is not a simple recapitulation of the developmental program producing PRs. Other regulators of LR initiation, acting independently of known pathways, are ARABIDILLO-1 and ARABIDILLO-2, which act redundantly to promote LR initiation in Arabidopsis (Coates et al., 2006). ARABIDILLOs are F-box proteins, suggesting that they form ubiquitin E3 ligases. Importantly, arabidillo mutants and ARABIDILLO-overexpressing plants are able to respond to exogenous auxin similarly to wild-type plants. In addition, auxin distribution in the root tip appears to be normal in arabidillo mutants, and auxin does not affect the nuclear localization of ARABIDILLO proteins (Coates et al., 2006; C. Nibau, J. Coates, unpublished). Transcriptomic comparison of wild-type, arabidillo mutant and ARABIDILLO-overexpressing roots reveals changes in some genes defined as pericycle-enriched and LR-enriched (Birnbaum et al., 2003; Levesque et al., 2006; https:// www.genevestigator.ethz.ch/), but no strong overlaps with other recent LR data sets defined by auxin induction, VFB signalling, LR emergence or red light signalling (Vanneste © The Authors (2008). Journal compilation © New Phytologist (2008) www.newphytologist.org New Phytologist (2008) 179: 595–614 601 602 Review Tansley review et al., 2005; Laskowski et al., 2006; Molas et al., 2006; Schwager et al., 2007; J. Coates, unpublished). ARABIDILLOs might act very early in determining pericycle cell fate. Given the recent suggestion that this determination occurs at the basal meristem (section III.1 ‘Which pericycle cells?’) it will be interesting to establish whether arabidillo mutants are affected in this process. 2. Redifferentiation to form a new meristem that recapitulates the root organization Lateral root primordium formation and emergence A series of well-characterized cell divisions gives rise to the LRP (Malamy & Benfey, 1997). The coordinated pattern of cell division is dependent on auxin signalling and on the activity of the PUCHI gene. PUCHI is expressed in pericycle cells that will form the LRP and in the LRP itself. PUCHI encodes an APETALA2 (AP2) transcription factor that is upregulated by auxin and acts downstream of auxin to restrict the area of cell proliferation within the LRP. PUCHI is also necessary for correct cell divisions within the LRP (Hirota et al., 2007). In rice, the EL5 RING finger ubiquitin E3 ligase maintains cell viability in the developing primordium. EL5 may act downstream of auxin, cytokinin and JA to prevent meristematic cell death (Koiwai et al., 2007). The identity of the target proteins and the involvement of EL5 in LRP hormone signalling pathways remain to be investigated. Once an LRP has initiated, it must form a functional meristem and emerge from within the parent root tissues. As a result of rounds of cell division, the LRP increases in size, forming a dome-shaped structure that penetrates the external cell layers of the PR. This requires separation of cells in the endodermis, cortex and epidermis for the passage of the LR to the outside (Fig. 4c,d). This process must be tightly regulated, as cell separation (particularly of the protective epidermal layer) constitutes a risk to the plant, potentially allowing the entry of pathogens from the soil into internal tissues. Much less is known about how LRs emerge than how they initiate. Changes in electrical potential occur around prospective sites of LR emergence (Hamada et al., 1992) and auxin seems to be required for LR emergence independently of its role in LR initiation. Shoot-derived auxin is required for LR emergence in Arabidopsis until c. 10 d after germination (Bhalerao et al., 2002), and auxin can induce root cell separation in Arabidopsis (Boerjan et al., 1995; Laskowski et al., 1995). Cell separation occurs via regulated activity of cell wallremodelling enzymes. Breakdown of pectin is particularly important for cell separation, as the middle lamella between adjacent cells is pectin-rich. Pectin is demethylated by pectin methylesterases (PMEs) before its catabolism. Pectin breakdown involves homogalacturonases called pectate lyases (PLAs). Interestingly, during LR emergence, the pectin in the emerging LR remains methylated, whereas the pectin in the overlying parent root tissues becomes demethylated, possibly in prepa- New Phytologist (2008) 179: 595–614 ration for its controlled breakdown as LRs emerge (Laskowski et al., 2006). How this differential pectin methylation is fully controlled remains an intriguing question. Various Arabidopsis studies have shown that cell wallremodelling enzymes are induced by auxin in roots (Neuteboom et al., 1999; Himanen et al., 2004; Vanneste et al., 2005; Laskowski et al., 2006). Cell wall remodelling genes induced by auxin include a PME, PLAs, and also an expansin and a beta-xylosidase (Laskowski et al., 2006). AtPLA1 and AtPLA2 are both upregulated steadily for up to 24 h after only a 15-min pulse of auxin: this response is blocked in the slr1/iaa14 mutant. In addition, expression of both AtPLAs is much higher in LR initials than in the pericycle cells from which they arise (Laskowski et al., 2006). The polygalacturonase (PG) family of cell wall-degrading enzymes may help to ‘prime’ the PR cells to separate ready for LR emergence (Gonzalez-Carranza et al., 2007). An Arabidopsis PG (PGAZAT) is expressed specifically in the cortical and epidermal cells overlying the future site of LR emergence. A pgazat insertion mutant has no obvious LR phenotype, but it is likely that functional redundancy exists. Interestingly, root PGAZAT expression is auxin-inducible (Gonzalez-Carranza et al., 2007). Activation of the lateral root meristem and lateral root elongation Activation and maintenance of the LR meristem requires polarized auxin transport to create an auxin maximum at the tip of the LRP: this requires regulated activity of auxin influx and efflux transporters. During LR development there is an important change in the direction of auxin flow, brought about by AUX/IAA-dependent repositioning of auxin efflux carriers towards the tip of the newly formed LR. This results in LR growth perpendicular to the PR (Benkova et al., 2003; Sauer et al., 2006). The new LRP auxin maximum regulates the activity of several transcription factors (Blilou et al., 2005). It is proposed that regulated expression of known regulators of PR meristem formation, such as the PLETHORA, CLAVATA, SCARECROW and SHORT ROOT, is also important for the maintenance of an active meristem in LRs downstream of auxin (for a recent review see Scheres, 2007). Because mutations in these genes severely impair PR growth, their effect on LR development has not been investigated: targeted overexpression and underexpression in LRs will clarify this issue. Abscisic acid can reversibly block meristem activation postemergence by inhibiting the cell cycle gene expression necessary for meristem activity, leading to LR growth arrest (De Smet et al., 2003). This effect of ABA defines a new auxin-independent checkpoint between LR emergence and meristem activation, which may also be regulated by nitrate levels (De Smet et al., 2003). In line with this observation, an ABA receptor mutant is completely insensitive to ABA inhibition of LR development (Razem et al., 2006). No other known ABA-insensitive mutants show insensitivity, suggesting www.newphytologist.org © The Authors (2008). Journal compilation © New Phytologist (2008) Tansley review Review mutations in the auxin efflux transporter MDR1 cause nascent LRs to arrest their growth (Wu et al., 2007). The ALF3 protein elevates the levels of auxin at the LRP, probably by facilitating auxin transport (Celenza et al., 1995). The auxin-induced homeobox gene HAT2 may also modulate auxin distribution within the primordium (Sawa et al., 2002). Despite the fact that cytokinins inhibit LR initiation, they have a positive effect on LR elongation in Arabidopsis and rice, possibly via stimulation of cell cycle gene expression in an auxin-independent process (Rani Debi et al., 2005; Li et al., 2006b). Fig. 5 Lateral root responses to nutrient deprivation. When nitrate (N) levels are high, lateral root (LR) emergence and elongation is represssed compared with normal conditions. Locally high levels of N promote local LR proliferation. In low phosphate (P), primary root growth ceases and LR density increases. In low sulphate (S), primary root growth and lateral root density increase, with LRs originating closer to the root tip. In low potassium (K), LR elongation is inhibited. that ABA signalling during LR emergence involves specific proteins (De Smet et al., 2003). ABI8, a plant-specific protein of unknown function, is a possible novel signalling candidate. abi8 mutant plants are less sensitive to ABA and, despite being able to initiate LR, their LR meristem soon loses competence to divide (Cheng et al., 2000; Brocard-Gifford et al., 2004). This checkpoint between LR emergence and meristem activation provides an elegant way by which environmental, nutritional and endogenous factors can modulate root architecture through ABA signalling (Signora et al., 2001; De Smet et al., 2006b; and section IV). For example, stress-induced oxylipin production affects LR development. Treatment of Arabidopsis seedlings with 9-hydroxyoctadecatrienoic acid (9-HOT), an oxylipin derivative, induces the accumulation of arrested early stage LRPs, accompanied by the upregulation of cell wall-associated genes (Vellosillo et al., 2007). The not-responding to oxylipins2 (noxy2) mutant has more LRs than the wild-type plant. 9-Hydroxyoctadecatrienoic acid and related oxylipins are probably endogenous modulators of LR emergence that may act via ABA signalling and they are involved in RSA reprogramming in response to pathogen infection (Vellosillo et al., 2007). Interestingly, ABA appears to have the opposite effect on LR emergence in legumes, stimulating LR formation in Medicago (Liang & Harris, 2005). The Medicago latd mutant has a reduced root surface area with short PRs, arrested LRPs and disorganized meristems (Bright et al., 2005). The latd phenotype can be at least partly rescued by the exogenous application of ABA, and latd mutants seem to be impaired in ABA perception or signalling (Liang et al., 2007). Lateral root elongation occurs by cell division and elongation from the meristem and is controlled by several factors. Auxin transport and signalling are important in this process. Auxin transport within the root is necessary for LR elongation, as IV. Plasticity: modification of lateral root development by the environment Plants are sessile organisms that need to survive in a dynamic environment. Consequently, their root systems need to maintain plasticity to react to fluctuating abiotic and biotic factors. Genetically identical plants can have very different RSA when grown in varying environmental conditions. Plants primarily respond to the abundance of macronutrients and water to produce the best root network for optimum growth and survival (Fig. 5). However, other exogenous factors, such as plant–pathogen interactions, are also important for root development. An overview of the current understanding of how changing external conditions affect RSA is presented here, with a particular focus on more recent advances. 1. Nitrogen availability and root system architecture: local and global effects Inorganic nitrogen Root adaptation to nitrogen levels is an excellent example of a plants’ developmental plasticity. Nitrogen is available in the soil as ammonia, nitrite, nitrate and organic nitrogen. The abundance of these compounds is highly variable and can have dramatic effects on LR development. Species-specific differences in nitrogen responses are apparent: LR length, number or both can be affected (Zhang & Forde, 1998; Linkohr et al., 2002; Boukcim et al., 2006). Nitrate levels have strongly opposing effects on LR growth, depending upon the context in which they occur. In low-nitrate soils, patches of high nitrate have a localized stimulatory effect on LR development in many species (Drew & Saker, 1975; Zhang & Forde, 1998). However, where nitrate levels are globally high (i.e. not growth limiting), LR growth is inhibited (Zhang et al., 1999). Thus, there are two clear morphological adaptations: a local stimulatory effect of exogenous nitrate supply on LR elongation, and a systemic inhibitory effect of high nitrate on LR meristem activation. This is caused by the signalling effect of nitrate itself, rather than being a response to downstream metabolites (Zhang & Forde, 1998). Some species, including barley and cedar, but not Arabidopsis, are also able to respond to a localized ammonium supply (Drew, 1975; Zhang et al., 1999; Boukcim et al., 2006). © The Authors (2008). Journal compilation © New Phytologist (2008) www.newphytologist.org New Phytologist (2008) 179: 595–614 603 604 Review Tansley review Key protein players specific to the ‘local nitrate’ response include the Arabidopsis NITRATE REGULATED-1 (ANR1) MADS-box transcription factor and the DUAL AFFINITY NITRATE TRANSPORTER (AtNRT1.1). Downregulation of ANR1 reduces LR stimulation in nitrogen-rich zones, without compromising the overall nitrate-induced inhibition of LRs (Zhang & Forde, 1998). Seven other MADS box genes have a similar expression pattern to ANR1 under different nitrate conditions (Gan et al., 2005). Three of these (AGL-16, AGL-21 and SOC1) interact with ANR1, although whether they represent nitrate signal transduction components is unknown (de Folter et al., 2005). AtNRT1.1 is induced by nitrate (Munos et al., 2004) and Atnrt1.1 mutants exhibit a strongly decreased response to local nitrate supply (Liu et al., 1999). Interestingly, this reduced responsiveness is accompanied by a reduction of ANR1 mRNA (Remans et al., 2006). Transporters have been previously identified as nutrient sensors, but it is unclear whether AtNRT1.1 is involved directly in nitrate sensing, or in facilitating access of nitrate to another sensor. High nitrogen inhibits LR development after emergence but before meristem activation. This effect is reversible: transferring plants to nitrate-limiting media results in a release of LR inhibition within 24 h, so plants can respond rapidly to fluctuating environmental nitrate levels (Zhang & Forde, 1998). A high shoot nitrate status is important for the inhibitory response, and an Arabidopsis mutant lacking nitrate reductase activity is hypersensitive to inhibition, suggesting that systemic accumulation of nitrate causes LR inhibition (Zhang et al., 1999). How are nitrate responses regulated during LR development? Various ABA-deficient Arabidopsis mutants have significantly reduced levels of LR inhibition in abundant nitrate (Signora et al., 2001). With both ABA and high nitrate, LRs are inhibited immediately after meristem activation (Signora et al., 2001; De Smet et al., 2003; and section III.1 ‘Other hormones affecting LR development’). Arabidopsis LR ABA-insensitive (LABI) mutants can still produce LRs in the presence of ABA: they are also less sensitive to high nitrate, implying that the inhibition of LRs by ABA and nitrate involves the same mechanism (Zhang et al., 2007a). Interestingly, transferring Arabidopsis and soybean from conditions of high nitrate to low nitrate increases root auxin (IAA) levels, suggesting that nitrate affects auxin synthesis or transport (Caba et al., 2000; Walch-Liu et al., 2000). Carbon : nitrogen (C : N) ratios affect RSA, further highlighting the complexity of the root response to nitrate. A high sucrose : nitrate ratio suppresses LRs, and a mutation in the high-affinity nitrate transporter AtNRT2.1 abolishes this inhibition (Malamy & Ryan, 2001; Little et al., 2005). Like AtNRT1.1, AtNRT2.1 may be a direct nitrate sensor (Little et al., 2005). In addition, AtNRT2.1 may have different functions depending on the degree and context of nitrate deficiency (Remans et al., 2006). New Phytologist (2008) 179: 595–614 Organic nitrogen Plants can use both organic nitrogen and inorganic nitrogen as a nutrient source. Arabidopsis roots show a specific set of responses to the amino acid l-glutamate, which inhibits PR growth and causes concomitant increases in LR density to varying degrees in different ecotypes (Walch-Liu et al., 2006). This response is similar to roots grown in low phosphate, forming a short and highly branched RSA (section IV.2; Williamson et al., 2001; Walch-Liu et al., 2006). Root responses to l-glutamate are accompanied by dramatic cytological changes, including microtubule depolymerization (Sivaguru et al., 2003). The PR tip is the sensor for l-glutamate (as with phosphate; section IV.2), which inhibits cell division in the meristem (Walch-Liu et al., 2006). Interestingly, the auxin transport mutant aux1 is somewhat insensitive to l-glutamate, whereas the axr1 mutant (a modifier of auxin signalling and possibly also other hormone pathways) is hypersensitive to l-glutamate, and various other auxin-signalling mutants exhibit wildtype sensitivity to l-glutamate (Walch-Liu et al., 2006). lglutamate probably acts as a signalling molecule rather than as a nutritional cue, because closely related amino acids do not elicit changes in root architecture (Walch-Liu et al., 2006). The molecular mechanism of l-glutamate perception at the Arabidopsis root tip remains to be discovered. Interestingly, rice with a mutant putative glutamate receptor (OsGLR3.1) has short PRs and LRs, reduced cell division, and premature differentiation and cell death in the root meristem (Li et al., 2006a). Carnitine, an organic nitrogenous cation, induces LR formation. However, disruption of an Arabidopsis plasma membrane-localized carnitine transporter, AtOCT1, led to increased root branching (Lelandais-Briere et al., 2007). AtOCT1 promoter activity is present in the root vasculature, including at sites of LR initiation. This suggests a possible modulatory role for carnitine movement or homeostasis in the control of RSA. It seems that AtOCT1 negatively regulates LR development, and the local concentration of carnitine in the root may affect the C : N ratio and hence LR development (Lelandais-Briere et al., 2007). 2. Phosphorous: modulating total RSA but sensed at the root tip Phosphorous is an essential nutrient, primarily taken up via the roots as inorganic phosphate (Pi). Phosphate is one of the most inaccessible macronutrients in the soil, as it forms insoluble compounds with metals in acidic and alkaline soils (Raghothama, 1999). Root system architecture modifications in response to phosphate are critical for the fitness of the plant and differ from those seen with nitrate, perhaps reflecting a Pi-foraging strategy, in contrast to nitrate responses that improve nitrogen uptake (Fitter et al., 2002). The main adaptive trait for accessing phosphate is the ability to explore different layers near the soil surface through www.newphytologist.org © The Authors (2008). Journal compilation © New Phytologist (2008) Tansley review changes in the RSA (Lopez-Bucio et al., 2000). Various adaptations have evolved in different plants. In Arabidopsis, Pi deficiency favours a redistribution of growth from the PR to LRs. The PR stops growing and the density and elongation of LRs increases, forming a shallow, highly branched root system (Williamson et al., 2001; Lopez-Bucio et al., 2002). This prevents further growth into less nutrient-rich deeper soils, increasing the exploration of the more nutrient-rich upper strata. In the bean Phaseolus vulgaris, a different strategy has evolved for achieving a similar explorative result: the angle of root growth is shifted to predominantly outwards instead of downwards when Pi levels are low (Bonser et al., 1996). The nitrogen-fixing white lupin forms proteoid (cluster) roots that secrete organic acids and phosphatases into the surrounding soil to solubilize phosphate and aid its uptake (Schulze et al., 2006). Unlike nitrate responses, the initial effect of low-Pi sensing is the arrest of PR growth, with changes in LRs occurring later. Loss of PR growth occurs via reduced cell elongation and a progressive loss of meristematic activity (Williamson et al., 2001; Sanchez-Calderon et al., 2005). The phosphate deficiency response-2 (pdr2) mutant displays hypersensitive inhibition of cell division in developing root meristems under Pi-limiting conditions, suggesting that PDR2 is required for meristem function where external Pi is low. It therefore represents a Pi-sensitive checkpoint that monitors Pi status and allows the root system to adjust accordingly (Ticconi et al., 2004). In addition to soil Pi status, systemic Pi levels may also be important for the induction of Pi-deficient RSA responses (Williamson et al., 2001). Active photosynthesis, or the presence of sugar, is also essential for RSA responses to limiting phosphate (Karthikeyan et al., 2007). Physical contact of the Arabidopsis PR tip with low-Pi medium is necessary and sufficient to arrest primary growth and reprogram root architecture (Svistoonoff et al., 2007). Multicopper oxidase mutants LOW PHOSPHATE ROOT-1 and -2 (LPR-1/-2) form long PRs in low Pi and provide evidence that the root cap has an important role in nutrient sensing. Interestingly, LPR1 was previously identified as a quantitative trait locus (QTL) important for phosphate responses (Reymond et al., 2006). Despite highlighting a novel role for multicopper oxidases in plant development, it is unknown whether LPRs are directly involved in the stimulation of LR growth in low Pi. A variety of hormones may modify the Pi response. Responses to low Pi correlate with increased auxin sensitivity and changes in auxin transport (Lopez-Bucio et al., 2002; Jain et al., 2007). Low phosphate resistant (lpr) mutants of BIG, a protein required for wild type levels of auxin transport, have reduced LRs in low Pi (Gil et al., 2001; Lopez-Bucio et al., 2005). However, neither BIG nor auxin transport is required for other RSA modifications seen in low Pi (Lopez-Bucio et al., 2005). Interestingly, many root responses to phosphate starvation are repressed by cytokinin signalling (Franco-Zorrilla Review et al., 2005). In addition, Pi starvation affects gibberellin signalling in roots, whereas gibberellin can attenuate the low-Pi response (Jiang et al., 2007). A variety of protein regulators of the phosphate-deficiency response have been uncovered, which affect transcription, translation and post-translational modifications. PHOSPHATE STARVATION RESPONSE-1 (PHR1) is an Arabidopsis MYB-like transcription factor that regulates a number of Pi-deficient responsive genes and is conserved in various plant species (Rubio et al., 2001). Miura et al. (2005) reported that PHR1 is a target of the small ubiquitin modifier (SUMO) E3-ligase AtSIZ1 in vitro. Interestingly, Atsiz1 mutants exhibit an exaggerated response to low Pi levels compared with wild type, most notably an extensive increase in LR development and a stronger PR inhibition (Miura et al., 2005). Although no direct link between PHR1 and RSA modification has been shown, two genes that belong to the PHR1 regulon (AtIPS1 and AtRNS1) are positively regulated by AtSIZ1 during the initial stages of Pi limitation (Miura et al., 2005). However, it is unknown whether the root phenotype of Atsiz1 mutants is a result of PHR1 modification and subsequent downstream gene expression, or whether the effect is pleiotropic, as AtSIZ1 also has roles in other developmental pathways (Jin et al., 2008). Other transcription factors identified, but not fully characterized as Pi-response components, include the basic leucine zipper (bZIP) transcription factor, PHI-2, in tobacco, and more recently OsPTF1, a bHLH transcription factor providing tolerance to low-Pi conditions in rice (Sano & Nagata, 2002; Yi et al., 2005). The WRKY75 transcription factor is strongly induced during Pi deprivation (Devaiah et al., 2007). Several genes are downregulated in plants with reduced levels of WRKY75, including high-affinity Pi transporters, which consequently leads to reduced phosphate uptake during Pi starvation (Devaiah et al., 2007). WRKY75 may be a specific modulator of LR development (rather than affecting the PR) and may also act independently of the Pi status of the plant to modify LR development (Devaiah et al., 2007). 3. Root responses to sulphur Sulphur, in the form of sulphate, is required for the synthesis of methionine and cysteine and is critical for cellular metabolism, growth and development, and stress responses. Sulphate deficiency is detrimental to a plant’s survival and leads to the development of a prolific root system, usually at the expense of shoot growth (Kutz et al., 2002). Sulphatedeficient roots elongate faster than those with sufficient sulphate, with LRs developing earlier, closer to the root tip and at a greater density (Kutz et al., 2002). This leads to an increase in total root surface area and a greater exploration of the soil. Sulphur deprivation leads to transcriptional activation of NITRILASE3 (NIT3), which converts indole-3-acetonitrile © The Authors (2008). Journal compilation © New Phytologist (2008) www.newphytologist.org New Phytologist (2008) 179: 595–614 605 606 Review Tansley review (IAN) to auxin (Kutz et al., 2002). Low sulphate-induced LRPs exhibit high NIT3 promoter activity, thus generating additional auxin close to the pericycle, allowing increased LR initiation (Kutz et al., 2002). Sulphur deficiency also upregulates the sulphate transporter genes SULTR1;1 and SULTR1;2 in the epidermis and cortex of roots (Yoshimoto et al., 2002); both transporters are reversibly downregulated in sulphate-replete conditions (Maruyama-Nakashita et al., 2004). A sulphur response regulatory element (SURE) is conserved in the upstream region of a variety of sulphate-deficient response genes, suggesting that RSA alterations in response to sulphur levels are coordinately controlled in Arabidopsis roots (Maruyama-Nakashita et al., 2004). Interestingly, SURE regions contain ARF consensus sequences, suggesting a role for auxin in the early sulphatestarvation response (Maruyama-Nakashita et al., 2004). A number of AUX/IAA genes have been implicated in the sulphate response, and transcriptomic analysis suggests that both auxin influx and IAA28 activity may modulate the response to low sulphate, perhaps by acting in a negative regulatory manner (Nikiforova et al., 2003, 2005). More recently, (Dan et al., 2007) suggested that auxin is involved in a subset of sulphurdeficiency responses, with other hormones (such as cytokinin and ABA) also playing a role. SULTR1 mRNA accumulation can be reduced by exogenous cytokinin, further suggesting points of regulation (Maruyama-Nakashita et al., 2004). 4. Potassium and lateral root development Lateral roots of potassium-starved plants arrest their elongation (Armengaud et al., 2004). Analysis of root transcriptomes from potassium-starved seedlings which were then resupplied with potassium revealed that certain genes were downregulated by potassium resupply, including stress-induced genes, transporters, calcium signalling components, sulphur metabolism components, and cell wall-remodelling enzymes. Conversely, upregulated genes were either transporters (including three root-specific nitrate transporters) or cell wallremodelling enzymes. The transcriptomic profile of potassiumstarved plants overlaps with sulphur starvation, but not with nitrate starvation or phosphate starvation, and also involves changes in jasmonate/defence signalling (Armengaud et al., 2004). Interestingly, the MYB77 transcription factor provides a direct link between potassium starvation responses and auxin signalling (Shin et al., 2007). 5. Water and salt stresses Water stress Water availability has a profound effect on a plant’s root system. Plant roots will grow towards wetter soil and away from high osmolarity (Takahashi et al., 2003). As water availability decreases (or osmotic stress increases), LR emergence is repressed, although LR initiation is largely unaffected (van der Weele et al., 2000; Deak & Malamy, New Phytologist (2008) 179: 595–614 2005; Xiong et al., 2006). This is likely to be an adaptive response encouraging increased water uptake from deeper soil layers. The molecular mechanisms underpinning the response are largely unknown, although ABA has an important role. The ABA-deficient mutants aba2-1 and aba3-2 have increased root system size compared with wild type under high osmotica (Deak & Malamy, 2005). Plants mutant for the LATERAL ROOT DEVELOPMENT 2 (LRD2) and Arabidopsis CYTPOLASMIC INVERTASE (AtCYT-INV1) genes also have a similar phenotype (Deak & Malamy, 2005; Qi et al., 2007). Alongside ABA, LRD2 may be required to determine the percentage of LRPs that become LRs under normal and stress conditions (Deak & Malamy, 2005). Abscisic acid and drought stress have similar and probably synergistic effects on LR development. Several drought inhibition of lateral root growth (dig) mutants have enhanced responses to ABA and are also drought tolerant, whilst others have a reduced LR-inhibition response to ABA and are drought sensitive (Xiong et al., 2006). DIG3 is particularly important for LR inhibition in response to ABA: dig3 mutants have normal LR growth under stress and are susceptible to drought. Interestingly, dig3 plants were smaller than wild-type plants under well-watered conditions, suggesting that the ABA and drought response involves factors required more generally for growth (Xiong et al., 2006). Drought tolerance in crop species is controlled by multiple QTLs (Nguyen et al., 2004): it will be interesting to discover whether dig loci define droughttolerant QTLs that are important for responding to water-stress in roots and globally. Salt stress Salt stress, which is related to drought stress, also reprograms RSA. Salt stress in Arabidopsis can induce root swelling with shorter total root lengths, a seriously reduced meristematic zone and a strong reduction in the number of LRPs, accompanied by the downregulation of several cell cycle genes (Burssens et al., 2000). However, salt stress may also trigger an increase in LR number. In chickpea (Cicer arietinum), the CAP2 (C. arietinum AP2) transcription factor is induced upon dehydration and binds to dehydration-response elements in many stress-inducible genes (Boominathan et al., 2004; Shukla et al., 2006). Transgenic tobacco expressing CAP2 is tolerant to salinity and osmotic stress, possibly because of a large increase in LR number (Shukla et al., 2006). Many auxin-response genes associated with LR development are upregulated in these plants, indicating links between salt stress responses and intrinsic auxin-associated development (Shukla et al., 2006). He et al. (2005) reported increased LR numbers and a reduction of PR length in response to high levels of NaCl in Arabidopsis. The NAC2 transcription factor is upregulated by NaCl and its overexpression causes increased LR formation specifically without a change in root length (He et al., 2005). NAC2 is upregulated by ethylene, auxin and ABA, and its induction by salt is compromised in auxin and ethylene www.newphytologist.org © The Authors (2008). Journal compilation © New Phytologist (2008) Tansley review signalling mutants (He et al., 2005). These data highlight the importance of phytohormone signalling in RSA responses to salinity. 6. Effects of light on root architecture Responding to light is key to plant survival. In addition to having profound effects on the seed and shoot, light can affect LR morphology. This can be direct (e.g. red light enhances LR formation via the COL3 gene) (Datta et al., 2006) or indirect, via effects in the shoot (Bhalerao et al., 2002). The bZIP transcription factor LONG HYPOCOTYL 5 (HY5) is a key player in light-induced development in Arabidopsis (Koornneef et al., 1980). Initially noted for defective light-induced hypocotyl elongation, hy5 mutants also have an elevated number of LRs, which grow faster than wild-type roots and are less responsive to gravity (Oyama et al., 1997). The hy5 root phenotype occurs as a result of the underexpression of two negative regulators of the auxin signalling pathway: AUXIN RESISTANT 2 (AXR2)/IAA7 and SOLITARY ROOT (SLR)/IAA14 (see section III.1 ‘Lateral root initiation requires auxin and regulated protein degradation’; Cluis et al., 2004). This interaction between HY5 and auxin signalling highlights the importance of both light-signalling networks and hormone-signalling networks in the control of RSA. HY5 also interacts with SALT TOLERANCE HOMOLOGUE 2 (STH2) (Datta et al., 2007). The sth2 mutant phenocopies the exaggerated root phenotype of the hy5 mutant, and the authors suggest that light-dependent inhibition of LRs by STH2 requires its binding to HY5, where it provides transactivating potential to the transcription factor (Datta et al., 2007). HY5 HOMOLOGUE (HYH) is a functional equivalent of HY5 with a similar expression pattern and responsiveness to light (Sibout et al., 2006). hyh mutants show wild-type RSA. However, hy5 hyh double mutants exhibit a suppression of the hy5 phenotype, displaying less prolific root growth than wild type (Sibout et al., 2006). It has been proposed that these double mutants represent the morphological response to a quantitative gradient in auxin signalling. This example suggests that the inactivation of genes, both of which affect the balance of a physiological process in the same manner, can result in very different morphological changes (Sibout et al., 2006). Molas et al (2006) examined total gene expression in dark-grown roots that were treated with red light for just 1 h. Interestingly, genes affecting cell wall metabolism and remodelling were consistently downregulated. Genes involved in hormone signalling (auxin, GA, ethylene) were also affected, as were proteins involved in intercellular transport, various transcription factors and several F-box proteins (Molas et al., 2006). Thus, light-induced changes in RSA are likely to happen rapidly and involve both signalling and remodelling processes. Review 7. Modulation of root architecture by biotic factors Within the soil, plants must compete and interact with a plethora of organisms, including microorganisms and other plant root systems. Roots secrete chemicals into the soil that affect other plant RSAs and also influence communication with microorganisms (Bais et al., 2004). In turn, viruses, bacteria and fungi can modify RSA. Many of these interacting species are pathogens and result in plant defence responses, while some can form symbiotic interactions leading to the formation of root nodules or mycorrhizas/proteoid roots (Autran et al., 2006; Oldroyd & Downie, 2006). In addition, soil microorganisms can produce auxin and cytokinin that dramatically affect RSA (see Section III) (Costacurta & Vanderleyden, 1995). Some recent advances in the molecular understanding of how pathogens modify RSA are presented in the following sections. Viral proteins Cucumber mosaic virus (CMV) infects a range of dicots, inducing developmental and growth abnormalities. The severity of disease symptoms is dependent on the CMV-2b protein (Lewsey et al., 2007). CMV-2b bypasses host defences both by inhibiting plant RNA silencing mechanisms (thus promoting the undetected spread of viral RNA) and by antagonizing salicylic acid signalling, which normally inhibits viral replication and cell-to-cell spreading. Arabidopsis infected with CMV or overexpressing CMV-2b show perturbed RSA, specifically, shorter PRs, increased LR density and increased LR length, leading to increased root surface area (Lewsey et al., 2007). Interestingly, CMV-2b stabilizes a number of endogenous Arabidopsis mRNAs that are targets of degradation by microRNAs (miRNAs), including the auxin signalling genes ARF17 and NAC1. Curiously, stabilized ARF17 is proposed to inhibit LR formation (Mallory et al., 2005), whereas NAC1 promotes LR development (Xie et al., 2000), suggesting that targeting of NAC1 may be particularly relevant during CMV infection. Cucumber mosaic virus ultimately inhibits root growth, but it is possible that transient increases in LR formation upon CMV infection are advantageous during initial virus infection and spread, because the presence of a higher number of emerging LRs and an increase in root surface area could provide a greater number of sites for virus entry. Pathogenic bacteria and fungi Pathogenic bacteria and fungi can directly influence LR development. Ralstonia solanacearum inoculation leads to reduced formation and elongation of LRs in petunia (Zolobowska & Van Gijsegem, 2006). Novel root lateral structures develop, derived from the pericycle founder cells that normally form LRs. These seem to act as colonization sites, and this process probably requires secreted bacterial proteins (Zolobowska & Van Gijsegem, 2006). The bacterium Pseudomonas syringae stimulates LR development and other auxin-related changes in Arabidopsis, © The Authors (2008). Journal compilation © New Phytologist (2008) www.newphytologist.org New Phytologist (2008) 179: 595–614 607 608 Review Tansley review whereas exogenous auxin promotes disease progression (Chen et al., 2007). The authors suggest that auxin could promote cell wall loosening. A Pseudomonas peptide was reported to downregulate auxin signalling, enabling disease resistance; however, the effect on LR development was not investigated (Navarro et al., 2006). The rice transcription factor OsWRKY31 is induced by rice blast fungus and also by auxin. Overexpression of OsWRKY31 confers resistance to rice blast fungus infection and also inhibits LR formation (Zhang et al., 2007b) In addition, OsWRKY31 upregulates auxin responsive genes, again linking auxin signalling and/or transport with the defence response (Zhang et al., 2007b). Interestingly, the nitrate-inhibitory effect on LR development is over-ridden when plants are inoculated with Phyllobacterium, a growth-promoting rhizobacterium (Mantelin et al., 2006). This effect was accompanied by altered expression of various transport genes, including AtNRT1.1. Continuing research in this new area will define the extent to which plant–pathogen interactions affect RSA. V. Transcriptomic studies to identify potential new regulators of lateral root development With the advent of high-throughput ‘omic’ experimental techniques, it is possible to augment molecular genetic studies of LR developmental mechanisms. This has included the generation of data sets of genes that are upregulated or downregulated specifically in different root cell types or in response to specific signals (see various sections above). In terms of probing cell type-specific gene expression in roots, studies from the Benfey laboratory have been influential. An initial study identified several hundred genes enriched in vascular tissues, including pericycle (Birnbaum et al., 2003). More recently, a high-resolution gene-expression map of all root cell types, including pericycle, xylem pole pericycle, phloem pole pericycle and LRPs, has been created (Brady et al., 2007). Analysis of this vast data set will provide new insights into the gene regulation occurring during LR development. For example, pericycle (in particular xylem pole pericycle) is enriched in mRNAs encoding cell wall-modifying enzymes, whereas genes encoding kinases and enzymes required for cell wall loosening are enriched in LRPs. In addition, auxin biosynthetic genes are enriched in pericycle and LRPs, and ABA signalling components are enriched in pericycle (Brady et al., 2007). A meta-analysis identifying indirect targets of the SHORTROOT (SHR) transcription factor uncovered a number of SHR-regulated genes that were enriched in or exclusive to pericycle (Levesque et al., 2006). It is thus tempting to speculate that SHR signalling pathways may regulate LR formation as well as PR development (Scheres et al., 2002), especially as similar signalling may regulate AR formation in pine trees and sweet chestnut trees (Sanchez et al., 2007). New Phytologist (2008) 179: 595–614 Specific cell types have been isolated from maize roots by laser capture microdissection (LCM) for transcriptomic and proteomic analysis (Woll et al., 2005; Dembinsky et al., 2007). Comparison of the pericycle transcriptome of wild-type maize with that of a mutant that cannot initiate LRs revealed that the majority of differentially expressed genes are involved in transcription or metabolism, or have unknown function. However, several genes involved in signal transduction (especially protein kinases), cell cycle regulation, cellular transport and defence were also identified (Woll et al., 2005). To identify genes involved in pericycle cell fate specification, rather than LR formation per se, pericycle cells were dissected from along the length of the root before the time that cell divisions occur (Dembinsky et al., 2007). The pericycle transcriptome and proteome was analysed, and further pericycle-enriched genes were isolated from cDNA libraries and expressed sequence tags (ESTs) (Dembinsky et al., 2007). Around 40 ‘pericycle-specific’ genes were identified, of which the largest two subsets were transcriptional regulators and unknown genes. Compared with vascular cells, pericycle appears enriched in genes involved in protein synthesis, but low in genes regulating cell fate. Twenty abundant soluble pericycle proteins were identified, of which 80% have a metabolic or energy function. There is only a small overlap between the LR initiation data set (Woll et al., 2005) and the pericycle data sets (Dembinsky et al., 2007), suggesting that specifying pericycle cell identity is a distinct process from forming a new LR. VI. Conclusions and future challenges A vast number of signals, both from within and outside the plant, impinge on the root to regulate its final architecture and branching pattern. Many challenges still exist for future ‘root biologists’. We must understand at the molecular level how these different signals work together to direct pericycle cell behaviour and later LR developmental processes. 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