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-PLANT August 2000 17/7/00 8:58 am Page 317 trends in plant science Research News Members of this clade are also found in gymnosperms but not ferns, suggesting a role in seed plant evolution10,11. One role of the foundation member, AG, is to specify the identity of carpels, an evolutionary novelty specific to the angiosperms10,11. Gene duplications creating the SHP genes could then have led to the evolution of dehiscence in the specialized fruits derived from the carpels and characteristic of Arabidopsis and other members of the Brassicaceae. The three closely related SEPALLATA genes fall within their own clade4,10,11. Originally named after the founding member AGL2, it now seems appropriate to rename this the SEPALLATA clade (Fig. 1). Again, this includes at least one gymnosperm MADS sequence, implying that one or more members played an ancient role in sporocarp development10,11. The fact that SEP genes are involved in specifying development of three floral whorls (one perianth and both reproductive whorls) in the angiosperm flower is consistent with such an ancient role. Practical implications Pod shatter before harvest is an important agronomic problem with cruciferous crops, especially canola (Brassica napus)13. One consequence of uncovering the role of SHATTERPROOF genes2, and of the FRUITFULL gene that regulates their expression6, is that tools now exist to modify the phenotype of the seed pod. It is possible that judicious modulation of the time and place of expression of these genes, and/or their targets, will allow seeds of canola to remain firmly encased until harvesting is ready to be carried out2,6. Acknowledgements I thank Marty Yanofsky, Sarah Liljegren and Soraya Pelaz for helpful comments, and for providing photographs of mutant plants. David Smyth Dept of Biological Sciences, Monash University, Melbourne, Vic 3800, Australia (tel 161 3 9905 3861; fax 161 3 9905 5613; e-mail [email protected]) References 01 Pelaz, S. et al. (2000) B and C floral organ identity functions require SEPALLATA MADSbox genes. Nature 405, 200–203 02 Liljegren, S.J. et al. (2000) SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404, 766–770 03 Riechmann, J.L. and Meyerowitz, E.M. (1997) MADS domain proteins in plant development. Biol. Chem. 378, 1079–1101 04 Alvarez-Bullya, E.R. et al. (2000) An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proc. Natl. Acad. Sci. U. S. A. 97, 5328–5333 05 Ma, H. et al. (1991) AGL1–AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Genes Dev. 5, 484–495 06 Gu, Q. et al. (1998) The FRUITFULL MADSbox gene mediates cell differentiation during Arabidopsis fruit development. Development 125, 1509–1517 07 Pneuli, L. et al. (1994) The TM5 MADS box gene mediates organ differentiation in the three inner whorls of tomato flowers. Plant Cell 6, 175–186 08 Angenent, G.C. et al. (1994) Co-suppression of the petunia homeotic gene fbp2 affects the identity of the generative meristem. Plant J. 5, 33–44 09 Ferrándiz, C. et al. FRUITFULL negatively regulates the SHATTERPROOF genes during Arabidopsis fruit development. Science (in press) 10 Hasebe, M. (1999) Evolution of reproductive organs in land plants. J. Plant Res. 112, 463–474 11 Theissen, G. et al. (2000) A short history of MADS-box genes in plants. Plant Mol. Biol. 42, 115–149 12 Ferrándiz, C. et al. (2000) Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development 127, 725–734 13 Spence, J. et al. (1996) ‘Pod shatter’ in Arabidopsis thaliana, Brassica napus and B. juncea. J. Microsc. 181, 195–203 The dawn of plant salt tolerance genetics Recent reports from Jian Kang Zhu et al. have provided clear evidence for a signal transduction pathway that mediates salt tolerance of plants by controlling ion homeostasis. Earlier research had identified several salt overly sensitive (sos) mutants of Arabidopsis thaliana ecotype Columbia, based on Na1/Li1 hypersensitivity1. Genetic complementation studies allowed the mutants to be placed into five allelic groups, sos 1–sos 5 (Refs 1,2). Phenotypic additivity analyses indicate that SOS1, SOS2 and SOS3 function in a common pathway, with SOS1 being epistatic to the other loci. Recently, mapped-based cloning and gene complementation has identified the genes at these three loci. SOS3 is a Ca21-binding protein that contains EF-hand structures and a myristoylation site in the N terminus3,4. It has greatest sequence homology with yeast calcineurin subunit B and with animal neuronal Ca21 sensors. SOS2 encodes a serine/threonine kinase with a catalytic domain similar to the yeast sucrose nonfermenting (SNF1) kinase and the mammalian AMP-activated protein kinase (AMPK), but is regulated differently through a distinctive C-terminal regulatory domain5. SOS1 is a putative plasma membrane Na1/H1 antiporter resembling the mammalian NHE and bacterial NhaP exchangers6. SOS signal pathway Molecular interaction, activation and site-specific mutant structure–function analyses indicate that SOS3 is required for the activation of the SOS2 kinase7. It is envisaged that SOS3 is the Ca21 sensor in a complex that is necessary for kinase activation. Myristoylation of SOS3 is required also for function in planta4. Mutations in SOS2 or SOS3 downregulate salt induction of SOS1 mRNA, indicating modulation of SOS1 transcription through some, as yet unknown, transcription factor6 (Fig. 1). However, mammalian NHE antiporters are regulated by phosphorylation, therefore SOS2 might regulate SOS1 additionally, independent of the transcription factor. Control of downstream effectors Participation of the Ca21-dependent SOS3 as the most upstream component of the known 1360 - 1385/00/$ – see front matter © 2000 Elsevier Science Ltd. All rights reserved. SOS pathway indicates that salt-stressresponse in plants, however perceived, involves a short regulatory cascade that includes elevated cytosolic Ca21 levels as an early event of the process2,8. As in yeast, the salt sensor and the initial signaling components controlling ion homeostasis have yet to be identified9. Presumably, Ca21 flux in microdomains near membranes initiate a signal, which implicates involvement of specific channels and tethered molecules that regulate channel function and transduce the signal intracellularly10,11. It is conceivable that SOS3 is one of the tethered molecules, and it might be useful to study how a local salt-induced Ca21 oscillation can activate a stress signal transduction pathway. A dual level of ion homeostasis regulation involving both transcriptional and post-translational mechanisms occurs in Saccharomyces cerevisiae12,13. This dual level of control over ion fluxes might be needed to allow survival upon both rapid stress imposition and continued growth during sustained elevated levels of external Na1. In the yeast salt-stress August 2000, Vol. 5, No. 8 317 -PLANT August 2000 17/7/00 8:58 am Page 318 trends in plant science Research News Xylem NHE Na Root SOS1 H+ Na+ ? TF H+ Vacuole Na+ Na+ ? Na+ SOS1 SOS2 ? Na+ Na+ Na+ NHE NHE H+ H+ Na+ Na+ Na+ Na+ + Na+ Na+ Na Na+ Na+ Transcriptional activation of SOS1 (and other effectors) + Leaf Ca2+ SOS3 H+ Vacuole Vacuole Casparian strip Trends in Plant Science Fig. 1. Model depicting the role of the salt overly sensitive (SOS) pathway in mediating salinity tolerance by controlling Na1 flux through SOS1. Abbreviations: TF, transcription factor; NHE, tonoplast Na1/H1 antiporter. Arrows with black arrowheads represent Na1 movement through unidentified flux system(s). Arrows with white arrow heads represent an antiporter system. Adapted from Ref. 8. signal pathway, the PP2B phosphatase calcineurin is a pivotal intermediate that controls transcription and activation of the ENA1 Ptype ATPase (Ref. 12; J.M. Pardo, unpublished), which is primarily responsible for Na1/Li1 efflux across the plasma membrane. It appears that the SOS3 protein might play a functionally similar role by both activating the transcription and in situ activity of the plasma membrane antiporter SOS1. An interesting divergence from the yeast model appears to be the activation through phosphorylation by SOS2 in plants and dephosphorylation by calcineurin in yeast. SOS pathway is probably multifunctional The calcineurin pathway in yeast is essential for regulation of key life cycle processes other than salinity tolerance, suggesting that salt stress response and adaptation are integrated into cellular homeostasis14,15. To date, the only salt tolerance effector controlled by the SOS pathway to have been identified is SOS1. However, the existence of numerous family members of both SOS2 and SOS3 in the Arabidopsis genome3,5–7,16 strongly indicates a focal involvement of SOS-family genes in other aspects of plant growth and development 318 August 2000, Vol. 5, No. 8 that are modulated by salt or even by other environmental cues. Different environmental perturbations could generate signals that are transduced through regulatory circuits that are composed of various members of the SOS gene families. Output from these pathways might also have rather specialized functions in stress adaptation processes, for example, determinants that modulate ion fluxes in the case of SOS2 and SOS3. In addition, more than one signal pathway might control the same output components. For example, calcineurin, HOG (high osmotic glycerol) signal pathways and, apparently, Ca21 signaling independent of calcineurin all regulate the activation of ENA1 (Refs 13,17). This redundancy probably reflects the multiple etiologies and pathologies associated with environmental perturbations, and the required integration that is intrinsic to cellular function. Identification of SOS determinants that are most essential for plant salt tolerance The existence of multigene families of SOS components reminds us that screening directly for phenotype change might be the approach that most rapidly identifies the family members that are most important to a particular phenotype. In fact, multiple alleles of sos1 and sos2 were identified in the hypersensitivity screen but not mutations to other members of the SOS1 or SOS2 families1. Furthermore, genetic, molecular interaction and activation data indicate that only specific isologs of the SOS families are pivotal determinants of salt stress adaptation. That is, all family members are probably not crucial to salt tolerance, at least during the developmental stage in which the hypersensitive mutants were identified. Functional interaction of specific family members must be confined to unique cell types expressing those members. The location of these cells in the organism de facto identifies sites of essential physiology necessary for whole plant adaptation and might provide important clues to the essential physiology of tolerance. A tentative model of the function of SOS1 (Ref. 6) in cells surrounding vascular elements is shown in Fig. 1. It is also conceivable that the specific cells, and particular SOS family members that are most essential for salt tolerance vary during ontogeny, to establish a correct pattern of physiology for adaptation. Systematic reverse genetics and knockout studies should also help to determine if SOS family members participate in response to other environmental stresses such as temperature or nutrient availability. Other possible osmotic stress signaling pathways in plants Other protein kinases, that are presumed to be focal intermediates in signal cascades, have been implicated in the salt stress response of plants, including Ca21-dependent protein kinases (CDPK), mitogen-activated protein kinases (MAPK), and SNF-like and Dbf2-like kinases. Although none of these protein kinases seems to regulate ion homeostasis specifically, their involvement in some aspect of the salt stress response is probable. Specific CDPKs transcriptionally regulate an osmotic stress responsive LEA (late embryogenesis abundant) gene (HVA1) that is an osmotic stress tolerance determinant18. An oxidative stress-activated MAPK [(NPK/ ANP) Nicotiana protein kinase/Arabidopsis homolog of NPK] pathway is implicated in enhanced abiotic stress tolerance because expression of the activated MAPKKK (mitogen-activated protein kinase kinase), NPK1, increases survival of seedlings in response to freezing, heat shock and hyperosmolarity or salt19. Apparently, the NPK/ANP pathway promotes stress tolerance independently of known cold- or osmotic-induced-stress signaling pathways, because activation does not lead to transcription of signature stressinduced genes. NPK1 has been implicated in cell cycle regulation. Salicylic acid-induced protein kinase (a MAP kinase) and an SNF-like Arabidopsis ASK1 ortholog are activated by hyperosmolarity20. The putative cell -PLANT August 2000 17/7/00 8:58 am Page 319 trends in plant science Research News cycle-regulated protein kinase At-DBF2 mediates salt and osmotic sufficiency, as well as heat and low temperature sufficiency, but does not mitigate oxidative stress effects21. DBF2 might be a component of the general transcription complex, analogous to CCR4 of yeast, which regulates expression of genes involved in osmotic and temperature tolerances. ATHK1 resembles the yeast osmosensor SLN1 that functions both as the sensor and receiver of the phospho-relay system that initiates the two-component HOG MAPK pathway that mediates hyperosmotic stress tolerance22. Yeast genetic suppression data indicate that ATHK1 can function as an osmosensor, although its role in plants has not yet been determined, and other components of the phospho-relay system or the signal cascade have not been identified. As genetic analysis of stress tolerance progresses, unexpected links between regulatory network(s) might come to light and further the knowledge base about the intersection of regulatory pathways. For example, the Arabidopsis mutant uvs66 is affected in the perception of signals triggered by genotoxic treatments (UV light and DNA-damaging chemicals)23. The uvs66 mutant is also hypersensitive to abscisic acid (ABA) and salinity. NaCl sensitivity is specific to Na1 because the mutant is resistant to high KCl and hyperosmolarity. Both SOS1 and UVS66 map to chromosome 2 but are not allelic because sos1 mutants are tolerant to UV light, DNAdamaging chemicals and ABA. The uvs66 mutant reveals crosstalk between ABA, Na1 homeostasis and response to genotoxic stress. Salt tolerance sufficiency The primary explanation for the slow inadequate progress towards understanding salinity tolerance has always been the complexity of this trait24. The research by Zhu and coworkers is an exemplary illustration of how genetics can lead to seminal dissection of a mechanistically complex phenotype. Several groups now use forward and reverse genetic approaches to identify determinants that mediate tolerance to salt, as well as other abiotic stresses. Soon, lists of stress tolerance determinants, both effectors and signal molecules, will be compiled on the basis of functional rather than correlative evidence. The genetics approach and application of genomics concepts is bringing the physiology of salt tolerance back from a cellular to an organismal focus. It is likely that the understanding of salt stress perception and adaptive responses of plants that lead to tolerance will be elucidated, rather than inferred, based on comparisons with unicellular models. However, it is also likely that another phase of the genetics approach will involve determining how the specific genes that control salt tolerance in model systems, such as Arabidopsis, differ from their orthologs in halophytic species. The identification of the halophytic versions of salt tolerance determinants will be facilitated greatly by the use of halophytes closely related to Arabidopsis thaliana, such as Arabidopsis (Thellungiella) halophila (Ref. 2). This species has considerable genetic orthology and will probably exhibit high synteny with Arabidopsis. At this point it is clear that genetic manipulation of crop plants for salt sufficiency should be possible. Acknowledgements We thank colleagues for informative discussion that helped in the preparation of this manuscript. We request the understanding of scientific peers whose papers were not cited owing to space constraints. Mike Hasegawa* and Ray Bressan 1165 Horticulture Building, Purdue University, West Lafayette, IN 47907-1165, USA Jose M. Pardo Consejo Superior de Investigaciones Cientificas, Instituto de Recursos Naturales y Agrobiologia de Sevilla, Campus de Reina Mercedes, Apartado 1052, Sevilla, Spain 41080 *Author for correspondence (e-mail [email protected]) References 01 Zhu, J.K. et al. (1998) Genetic analysis of salt tolerance in Arabidopsis: evidence for a critical role of potassium nutrition. Plant Cell 10, 1181–1191 02 Zhu, J.K. Genetic analysis of salt tolerance using Arabidopsis thaliana. Plant Physiol. (in press) 03 Liu, J. and Zhu, J.K. (1998) A calcium sensor homolog required for plant salt tolerance. Science 280, 1943–1945 04 Ishitani, M. et al. SOS3 function in plant salt tolerance requires N-myristoylation and calciumbinding. Plant Cell (in press) 05 Liu, J. et al. (2000) The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc. Natl. 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Chem. 269, 8792–8796 13 Mulet, J.M. et al. (1999) A novel mechanism of ion homeostasis and salt tolerance in yeast: the Hal4 and Hal5 protein kinases modulate the Trk1–Trk2 potassium transporter. Mol. Cell. Biol. 19, 3328–3337 14 Garrett-Engele P. et al. (1995) Calcineurin, the Ca21/calmodulin-dependent protein phosphatase, is essential in yeast mutants with cell integrity defects and in mutants that lack a functional vacuolar H1-ATPase. Mol. Cell Biol. 15, 4103–4114 15 Mendoza I. et al. (1996) Activated calcineurin confers high tolerance to ion stress and alters the budding pattern and cell morphology of yeast cells. J. Biol. Chem. 271, 23061–23067 16 Kudla, J. et al. (1999) Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by stress signals. Proc. Natl. Acad. Sci. U. S. A. 96, 4718–4723 17 Danielsson, A. et al. (1996) A genetic analysis of the role of calcineurin and calmodulin in Ca21dependent improvement of NaCl tolerance of Saccharomyces cerevisiae. Curr. Genet. 30, 476–484 18 Sheen, J. (1996) Ca21-dependent protein kinases and stress signal transduction in plants. Science 274, 1900–1902 19 Kovtun, Y. et al. (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc. Natl. Acad. Sci. U. S. A. 97, 2940–2945 20 Mikolajczyk, M. et al. (2000) Osmotic stress induces rapid activation of a salicylic acidinduced protein kinase and a homolog of protein kinase ASK1 in tobacco cells. Plant Cell 121, 165–178 21 Lee, J.H. et al. (1999) A highly conserved kinase is an essential component for stress tolerance in yeast and plant cells. Proc. Natl. Acad. Sci. U. S. A. 96, 5873–5877 22 Urao, T. et al. (2000) Two-component systems in plant signal transduction. Trends Plant Sci. 5, 67–74 23 Albinsky, D. et al. (1999) Plant responses to genotoxic stress are linked to an ABA/salinity signaling pathway. Plant J. 17, 73–82 24 Hasegawa, P.M. et al. (2000) Plant cellular and molecular responses to high salinity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 463–499 August 2000, Vol. 5, No. 8 319