Download The fruit, the whole fruit, and everything about the

Journal of Experimental Botany, Vol. 65, No. 16, pp. 4491–4503, 2014
doi:10.1093/jxb/eru144 Advance Access publication 10 April, 2014
Review paper
The fruit, the whole fruit, and everything about the fruit
Sofia Kourmpetli1 and Sinéad Drea1,*
1 Department of Biology, University of Leicester, University Road, Leicester LE1 7RH, UK
* To whom correspondence should be addressed. E-mail: [email protected]
Received 14 January 2014; Revised 14 January 2014; Accepted 5 March 2014
Abstract
Fruits come in an impressive array of shapes, sizes, and consistencies, and also display a huge diversity in biochemical/metabolite profiles, wherein lies their value as rich sources of food, nutrition, and pharmaceuticals. This
is in addition to their fundamental function in supporting and dispersing the developing and mature seeds for the
next generation. Understanding developmental processes such as fruit development and ripening, particularly at the
genetic level, was once largely restricted to model and crop systems for practical and commercial reasons, but with
the expansion of developmental genetic and evo-devo tools/analyses we can now investigate and compare aspects
of fruit development in species spanning the angiosperms. We can superimpose recent genetic discoveries onto
the detailed characterization of fruit development and ripening conducted with primary considerations such as yield
and harvesting efficiency in mind, as well as on the detailed description of taxonomically relevant characters. Based
on our own experience we focus on two very morphologically distinct and evolutionary distant fruits: the capsule of
opium poppy, and the grain or caryopsis of cereals. Both are of massive economic value, but because of very different
constituents; alkaloids of varied pharmaceutical value derived from secondary metabolism in opium poppy capsules,
and calorific energy fuel derived from primary metabolism in cereal grains. Through comparative analyses in these
and other fruit types, interesting patterns of regulatory gene function diversification and conservation are beginning
to emerge.
Key words: Capsule, cereals, fruit, grain, metabolism, poppy.
Introduction
The fruit: from initiation to utilization
The ability to conduct research on myriad aspects of fruit
development from organ initiation through development to
usable end product (Fig.1) in phylogenetically and morphologically diverse species that have agricultural, medicinal,
and ecological value provides an opportunity to comprehensively understand the fruit and its origin in the plant
kingdom. The story of the fruit poses intriguing questions
for every biological discipline to address, as well as posing
questions at multiple levels of analyses (Fig. 1). As a notable
botanical innovation in the arrival of the angiosperms, to
being the primary human food source, the characterization
of each chapter in the story of the fruit requires taxonomists, developmental biologists, bioinfomaticians, biochemists, and botanists. The links between the different levels of
investigation, particularly taxonomy, phylogeny, and development are becoming stronger in the area of comparative
development or evolution of development. Biologists have
always been interested in the evolution of developmental
processes, but advances in molecular techniques now complement earlier analyses, which were inevitably descriptive
and based on gross morphological characteristics. The
ability to extract and sequence DNA from diverse species
is still the staple of phylogenetic analyses, but advances in
sequencing technology and adaptation of other molecular
technologies has taken phylogenetic analysis into a whole
new era to the point that the concept of ‘model organism’ is
becoming commonplace, at least to some degree depending
on the definition of what constitutes a ‘model’ (Abzhanov
et al., 2008; Rowan et al., 2011). There is perhaps still a
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4492 | Kourmpetli and Drea
Fig. 1. Flowchart illustrating the many levels at which research on fruits can be conducted depending on the focus of individual groups, from initiation
to point of harvesting and processing. Some specific developmental processes, metabolic products and cell/tissue types are included. (This figure is
available in colour at JXB online.)
distance between developmental studies focusing on early
stages in fruit development and the metabolic/biochemical
analysis of the end product. However, at some point downstream in the fruit’s genetic regulatory network (GRN), the
master regulators at the top of the hierarchy that control
organ identity, specification, and development of specialized fruit tissues (Table 1) must link to the ‘local’ regulators
of specific metabolic and biochemical pathway components.
In the case of AGAMOUS (AG), the MADS-box gene specifying carpel identity in Arabidopsis, a recent systematic
identification of its targets using extensive transcriptomic
data highlighted that a large proportion of direct targets
were also transcription factors (TFs), including CRABS
CLAW (CRC), the YABBY gene also important in fruit
development (O’Maoileidigh et al., 2013). Diversification
in regulatory gene expression and/or function anywhere in
this chain undoubtedly accounts for the massive variation
in plants generally and fruits specifically (Carroll, 2008).
Comparative analyses across the angiosperms using key
regulator genes (Table 1) as candidates is revealing intriguing patterns of conservation and diversification in function
high up in this regulatory hierarchy.
In this review we focus on two cultivated fruit types we
have been involved with directly, the poppy capsule and the
cereal grain. Fig. 2 puts these case studies in the context of
the angiosperm phylogeny, and in this review we summarize
research that encompasses basic development and its applied
relevance (Fig. 1). Our focus is on the TFs controlling these
diverse processes from initiation to end-use. As traits selected
for through agriculture involve fundamental plant developmental processes, it is not surprising that TFs are being identified as the determinants of these processes and the bases
of the genetic differences distinguishing wild and cultivated
species (Doebley et al., 2006; Tables 1 and 3).
Most of the work published on the genetic basis of fruit
development in eudicot species has been focused on core eudicots, such as the model Arabidopsis, crop tomato, and ornamental Petunia (Table 1). However, given the wide diversity
of fruit forms and the practical/economic significance of key
fruit traits in commercially important species (abscission,
dehiscence, ripening duration, longevity, seed production), a
more detailed study of fruit development in other angiosperm
groups, such as basal eudicot species, is extremely interesting
from an evolutionary point of view. The order Ranunculales
represents the earliest diverging eudicot order and includes
species that show a great variety of flower and fruit forms.
Within this order, the Papaveraceae and Ranunculaceae
families are the focus of recent research (Table 2). In addition, in terms of cereal research, Brachypodium distachyon
has been emerging in the last few years as a valuable model
species and a taxonomically relevant reference point for the
‘core pooids’, such as wheat, barley, and oat. With its genome
already sequenced and several genetic resources already available (IBI, 2010; Mur et al., 2011), a better understanding of
its fruit development at a molecular genetics level could help
shed light on more complex genomes, such as wheat, and ultimately assist in the genetic improvement of temperate grasses.
Case study: the capsule of Papaver
somniferum (opium poppy), a basal eudicot
Within the Ranunculales, there are very diverse fruit forms
(Table 2). The capsule of opium poppy contrasts to the explosive silique-like fruit of California poppy (Becker et al., 2005).
Each species (Table 2) has features that are both shared and
distinct from the other, and from the established model species
in the core eudicot and monocot clades, such as Arabidopsis,
Fruit development in poppy and cereals | 4493
Table 1. A summary of some of the key fruit developmental genes identified in core eudicots and being examined in species across the
angiosperms
The list is by no means complete but includes genes that cover a range of constituent tissues related to fruit development and where we aim to
highlight recent findings.
Location
Gene name
Genus
TF family
Function/
tissue
Reference
Carpel/
fruit
AG
TAG1
pMADS3
FAR
SHP1/2
FBP6
PLE
TAGL1
FUL
FUL1 (TDR4)
FUL2(MBP7)
RIN
AGL63/GOA
RPL
IND
ALC
AP2
AP2a
CRC
FAS
FBP7/11
STK
INO
TT16/ABS
Arabidopsis
Tomato
Petunia
Antirrhinum
Arabidopsis
Petunia
Antirrhinum
Tomato
Arabidopsis
Tomato
Tomato
Tomato
Arabidopsis
Arabidopsis
Arabidopsis
Arabidopsis
Arabidopsis
Tomato
Arabidopsis
Tomato
Petunia
Arabidopsis
Arabidopsis
Arabidopsis
MADS-box
MADS-box
MADS-box
MADS-box
MADS-box
MADS-box
MADS-box
MADS-box
MADS-box
MADS-box
MADS-box
MADS-box
MADS-box
Homeobox
HLH
HLH
AP2/EREBP
AP2/EREBP
YABBY
YABBY
MADS-box
MADS-box
YABBY
MADS-box
Identity, determinacy
Identity, determinacy
Development
Development
Valve margin
Development
Identity
Ripening/composition
Valve shattering
Ripening
Ripening
Ripening/composition
Fruit cell size
Replum - shattering
Dehiscence
Dehiscence
Replum
Ripening/composition
Polarity, determinacy
Locule number (size)
Identity/determinacy
Seed dispersal
Integument
Integument
Yanofsky et al., 1990
Pnueli et al., 1994
Tsuchimoto et al., 1993
Davies et al., 1999
Liljegren et al., 2000
Heijmans et al., 2012
Bradley et al., 1993
Pan et al., 2010; Vrebalov et al., 2009
Gu et al., 1998
Bemer et al., 2012
Bemer et al., 2012
Vrebalov et al., 2002
Prasad et al., 2010
Roeder et al., 2003
Liljegren et al., 2004
Rajani and Sundaresan, 2001
Ripoll et al., 2011
Chung et al., 2010; Karlova et al., 2011
Bowman and Smyth, 1999
Cong et al., 2008
Colombo et al., 1995; Heijmans et al., 2012
Pinyopich et al., 2003
Villanueva et al., 1999
Nesi et al., 2002
Ovule/
seed
tomato, and rice, and they therefore offer much material
for morphological comparisons to models and crop species.
The ovary of Papaver somniferum is globular and supported
on a gynophore and receptacle subtended by the pedicel
(Fig. 3). It is overlaid by a flat persistent stigmatic surface
composed of rays that are fused at the edges and separated
by deep invaginations producing stigmatic lobes. Profuse
papillae that capture the dehisced pollen grains are found
at the ray edges. There is no style. The capsule is designated
as poricidal in terms of seed dispersal, the pores forming
just beneath the stigmatic rays; however, the capsules can
be dehiscent or indehiscent as not all cultivars produce
pores. The gynoecium is multicarpellate paracarpous and
the edges of the fused carpels form adaxial septae that do
not extend across the fruit centre producing a unilocular
capsule. The number of stigmatic rays equals the number
of carpels. The capsule is open valvate along placentae with
distinct valves visible. Numerous ovules develop on the placentae covering the surface of the septae and seeds vary in
colour from white to black (Bernath, 1998; Grey-Wilson,
2000; Kapoor, 1995).
One of the main drivers in developing functional tools
in basal eudicot species is to explore the genetic basis of
the development of the varied flower morphologies, and
to ascertain at the functional level the degree of conservation or divergence in the genetic mechanisms directing the
initiation, specification, and development of the flower and
its composite organs. Clues to these were already obtained
using detailed spatial and temporal gene expression analyses
in addition to phylogenetics and taxonomy (e.g. Kramer and
Irish, 1999; Drea et al., 2007). Within the basal eudicots there
are published reports of at least six species being amenable
to explicit functional gene studies using VIGS (virus-induced
gene silencing; Di Stilio et al., 2010; Goncalves et al., 2013;
Gould and Kramer, 2007; Hidalgo et al., 2012; Hileman
et al., 2005; Table 2), in addition to the use of mutagenized
lines and natural variants (Galimba et al., 2012; Lange et al.,
2013), and all have some genomic resources in place and/or
in development (Becker et al., 2005; Di Stilio et al., 2005;
Kramer, 2009).
When considering specific genes through which to compare genetic mechanisms of flower and fruit development
in basal eudicots, it is not surprising that members of the
ABC(DE) model of flower development derived from early
work in Arabidopsis, Antirrhinum, and Petunia (Coen and
Meyerowitz, 1991; Heijmans et al., 2012; Ferrario et al.,
2004) were prime candidates (Table 2). In relation to fruit
development we focus on the studies involving C/D-class
analyses in addition to genes from other families because
of their expected role in fruit development (Table 1). The
MADS-box genes involved in fruit development pose
interesting schemes in terms of phylogenetics as well as in
terms of the very different fruit forms and their developmental programmes. For example, the SHATTERPROOF
4494 | Kourmpetli and Drea
Fig. 2. Simplified land plant phylogeny (based on figure in Rowan et al., 2011) to indicate basic relationships of various genera and species discussed.
(SHP) C-class and APETALA 1 (AP1) A-class sub-lineages are only found in core eudicots where they control
fruit patterning and outer whorl identity in Arabidopsis,
respectively (Dreni and Kater, 2014; Kramer et al., 2004,
Litt and Irish, 2003). AG orthologues have been studied at
the functional level in P. somniferum, Eschscholzia californica, and Thalictrum thalictroides. Analyses of AG genes
in these species showed the depth of C-functional conservation (Galimba et al., 2012; Hands et al., 2011; Yellina
et al., 2010). In Eschscholzia and Thalictrum duplication
has generated two AG paralogues that in Eschscholzia have
similar expression profiles (Zahn et al., 2006) and functional
redundancy, whereas in Thalictrum one of the paralogues,
ThAG2, is expressed in ovules only (Di Stilio et al., 2005).
The other ThAG1 paralogue is required for AG floral identity and determinacy functions (Galimba et al., 2012). In
opium poppy, alternative splicing at the AG locus generates
two transcripts with similar expression and a requirement
for both transcripts to mediate the identity and determinacy
functions (Hands et al., 2011).
Orashakova et al. (2009) studied the role of CRC in
detail in Eschscholzia, showing that the gene played a
role not only in fruit development and determinacy as
in Arabidopsis, but also in ovule development. The FUL
genes have been characterized functionally in both P. somniferum and E. californica, where it was shown that the
duplicated FUL genes retained the collective roles of the
paralogous euAP1 and euFUL in meristem, petal identity,
and fruit (where they mediate differentiation of the valve;
Gu et al., 1998). Based on these results subfunctionalization was proposed as the consequence of the duplication
in the core eudicots (Pabon-Mora et al., 2012; Table 2).
Intriguingly, the FUL genes in Aquilegia showed no role in
fruit development and the authors suggested that the floral
and reproductive functions were decoupled in this species
(Pabon-Mora et al., 2013).
The P. somniferum (opium poppy) capsule as a source
of alkaloids
As a group of plants the Ranunculales are also distinctive
in that they are the main producers of the BIA (benzylisoquinilone alkaloid) compounds with E. californica, P. somniferum, and Thalictrum (flavum and tuberosum) being some
of the most intensively studied species in this regard (Ziegler
and Facchini, 2008). BIAs are specialized metabolites that
are often associated with powerful pharmacological effects
including analgesic, antibacterial, relaxant, cough suppressant, and anticancer properties (Hagel and Facchini, 2013).
Opium poppy is distinctive in its production of the valuable
morphinan alkaloids including thebaine, codeine, and morphine, which are the main components of its latex. The latex
is essentially the cytoplasm of specialized cells called laticifers; specific to certain families throughout the angiosperms
and classified based on their development and morphology
(Hagel et al., 2008). Esau (1953) classified the laticifers of
Papaver as being articulated anastomosing—chains of cells
(forming vessels), where the end walls are perforated and further connected to other vessels. They are located adjacent to,
and develop simultaneously with, the phloem tissue (Hagel
et al., 2008) and their path is followed by tracking the course
of the vascular bundle.
The opium poppy’s capsular fruit is synonymous with
alkaloid production (Fig. 3). Alkaloid biosynthesis is not
Fruit development in poppy and cereals | 4495
Table 2. A summary of recent basal eudicot research highlighting functional analyses of flower genes in Ranunculales
Family
Genus
Fruit features
Flower genes studied
Reference
Papaveraceae
Eschscholzia
Bivalved, explosive
FLO, MADS-box (AP3,
PI, AG, FUL), YABBY (CRC)
Papaver
Poricidal capsule
MADS-box (AP3, PI, AG,
FUL), YABBY (FIL)
Cyscicapnos
Thalictrum
Bicarpellate, balloon-like
Open, uniovule, ascidiate
FLO
MADS-box (AG)
Aquilegia
apocarpic
MADS-box (AP3, PI, FUL)
Nigella
Inflated, capsule; syncarpous
MADS-box (AP3)
Orashakova et al., 2009;
Pabon-Mora et al., 2012;
Wege et al., 2007; Yellina
et al., 2010
Pabon-Mora et al., 2012;
Drea et al., 2007; Hands
et al., 2011; Vosnakis
et al., 2012
Hidalgo et al., 2012
Di Stilio et al., 2010;
Galimba et al., 2012
Kramer et al., 2007;
Pabon-Mora et al., 2013
Goncalves et al., 2013
Ranunculaceae
Table 3. Summary of some key TFs identified in grasses affecting various aspects of grain number, specification, development,
composition, and harvesting
Location
Gene name
Genus
TF Family
Function
Reference
Arabidopsis
orthologue
Surrounding tissues
NUD
TGA1
qSH1
SH4*
AP2(SHAT1)
SH1
Q
VRS1
HvAP2
DL
OsMADS3/58
Hordeum
Zea
Oryza
Oryza
Oryza
Sorghum
Triticum
Hordeum
Hordeum
Oryza
Oryza
AP2/EREBP
SBP-binding
homeobox
Myb-like
AP2/EREBP
YABBY
AP2/EREBP
HD-ZIP
AP2/EREBP
YABBY
MADS-box
Adhering hull (palea/lemma)
Seed casing (cupule)
Grain shattering
Grain shattering
Grain shattering
Grain shattering
Grain size
Two-row to six-row barley
Grain density
Carpel identity
Carpel development
WIN1/SHN1
OsMADS13/21
GT1
Oryza
Zea
MADS-box
HD-ZIP
Ovule identity
Carpel development and number
RC
RSR1
OSMADS29
ZmMRP-1
OPAQUE2
Oryza
Oryza
Oryza
Zea
Zea
HLH
AP2/EREBP
MADS-box
Myb
bZIP
BLZ1/2
HvMYBS3
GAMYB
BPBF
SAD
MCB1
Hordeum
Hordeum
Hordeum
Hordeum
Hordeum
Hordeum
bZIP
Myb
Myb
DOF
DOF
Myb
Grain colour (pericarp)
Starch
Nucellus degradation
Transfer cell differentiation
Storage protein
gene activation
Storage protein/gene activation
GA response/germination
GA response
GA response
GA response
GA response
Taketa et al., 2008
Wang et al., 2005
Konishi et al., 2006
Li et al., 2006
Zhou et al., 2012
Lin et al., 2012
Simons et al., 2006
Komatsuda et al., 2007
Houston et al., 2013
Yamaguchi et al., 2004
Yamaguchi et al., 2006;
Dreni et al., 2011
Dreni et al., 2007
Whipple et al., 2011;
Wills et al., 2013
Sweeney et al., 2006
Fue and Xue, 2010
Yin and Xue, 2012
Gomez et al., 2002, 2009
Hartings et al., 1989
Shattering from rachis
Grain number/size
Carpel/ovule
Endosperm domains
restricted to the capsule, however, and alkaloids are produced throughout the poppy plant after the laticifers have
differentiated in the seedlings. At the base of the capsule the
vascular bundles fuse forming several amphicribral (where
the xylem is surrounded by phloem) bundles (Kapoor, 1973;
Fukuda, 2004), and the organization and concentration of
RPL
AP2
YAB2
AtTOE1
ATHB-21
AP2
CRC
AG
STK
TT8
AP2
AGL32/ABS
BZO2H3
Onate et al., 1999
Diaz et al., 2002
Mena et al., 2002
Isabel-LaMoneda et al., 2003
Rubio-Somoza et al., 2006
MYB33/65/101
the vascular tissue and associated laticifers contributes to
proficient latex production in the fruit. The seeds are actually free from alkaloids as the laticiferous vessels terminate
in the placenta and do not follow through to the developing
ovule. The seeds produced by the capsule are also familiar as
toppings for bagels and other bread products, and are rich
4496 | Kourmpetli and Drea
Fig. 3. Papaver somniferum (opium poppy). Left; photograph of a flower of cultivar Persian white with inset of solitary capsule. Right; schematic showing
capsule in longitudinal profile and capsule in transverse profile. A close-up of the vascular bundle and laticifers is shown bottom right. Drawings based on
Petri and Mihalik (1998), Kapoor (1995), and Ziegler and Facchini (2008).
in oils that can also be used in producing paints and varnishes (Bernáth, 1998a). Whereas the production of many
alkaloids can be induced in cell cultures, this has only been
successful for sanguinarine in opium poppy, and not for the
morphinan alkaloids (Zulak et al., 2008), and so the cultivation of opium poppy plants is still an essential part of morphine production. This has been suggested to be because
the cell cultures do not possess the differentiated laticifers
present in seedlings and older plants (Kutchan et al., 1983).
When the flower opens the already large capsule continues
to increase markedly in size for three weeks with the vertical section area of the capsule increasing more than 3-fold
within the first week (Kapoor, 1995). Images of lanced capsules oozing latex are commonly used to illustrate the process of how opium and alkaloids are obtained from the plant,
and this still continues to be the means of harvesting in some
areas (Bernáth, 1998b). Two weeks after petal fall the capsule
has reached its maximum size, but is still green, and it is at
this point that the first incision or lancing is performed. The
instrument used is a knife with three or four blades about
2 mm apart, and the capsules are scored longitudinally to
or from just below the stigmatic rays (Kapoor, 1995). The
depth of incision is vital, as if scored too deeply the latex
can seep internally, contaminating seeds (CONTAM, 2011),
rather than aggregate externally on the surface of the capsule
from where it is collected. However, this massively laborious
and intricate means of extraction has been superceded by
the Kabay method (named after the Hungarian chemist who
developed the process) in which the alkaloids are retrieved
from poppy ‘straw’ (Németh, 1998) by mechanical harvesting
using modified combine harvesters. In this method the poppy
capsules and 10–20 cm of the stem are harvested, allowed to
dry completely, and seeds separated before processing the
remaining material.
The knowledge that alkaloids were associated with the latex
led to the gradual identification of the many intermediates
and enzymes in the alkaloid biosynthetic pathway. A recent
review of BIA biosynthesis (Hagel and Facchini, 2013) listed
25 enzymes in the intricate biosynthetic pathways of the BIAs
berberine, morphine, sanguinarine, codeine, and thebaine for
which corresponding genes have been identified. This provided the means (probes and antibodies) to map the synthesis
sites of the alkaloids leading to the discovery that the sieve elements of the phloem were directly involved (Bird et al., 2003;
Weid et al., 2004). This was a significant discovery implicating
sieve elements in complex metabolic processes and not just
transport of solutes. As well as facilitating the discovery of
much about the nature of laticiferous vessels and the proactive role of phloem in plant metabolism, the biosynthesis of
alkaloids in poppy capsules also enhanced our understanding
of genomic features that underlie the production of natural
substances in plants. Comparative transcriptomics using a
high-noscapine yielding cultivar identified the biosynthetic
enzymes organized as a gene cluster in the genome (Winzer
et al., 2012). This study provided another example of the
association of the biosynthesis of natural plant products
with gene clusters such as avenicin in oat roots (DellaPenna
and O’Connor, 2012). It is satisfying that much of this recent
progress in characterizing the BIA biosynthesis pathways and
its components in opium poppy has been facilitated by the
development of tools for evo-devo analyses such as VIGS,
though there are caveats and limitations with this technique
when studying either BIA biosynthesis or developmental control genes (Hagel and Facchini, 2013; Geuten et al., 2013).
Case study: the grain of temperate cereals
The fruit of the grasses is as distinctive botanically as it is valuable economically. In contrast to fleshy-fruited crops such
as tomato and the alkaloid-producing capsule of poppy, it
is the single seed within the fruit that holds the economically
Fruit development in poppy and cereals | 4497
valuable starch and protein reserves. In the maturing caryopsis the fruit pericarp is reduced to just a few layers of largely
collapsed cells and the cuticle-encased inner integument of the
seed (Esau, 1960). It is the ‘shattering’, ‘threshing’, and ‘winnowing’ procedures that separate flower from fruit in cereal
terminology i.e. separating the grain both from the pedicel
at the base and from the adhering lemmae and palea (husk/
hull). Through milling, the bran (remaining pericarp, integuments, and aleurone) is further separated from the central
endosperm. In considering fruit development and ripening in
the context of the cereal grain, therefore, the surrounding floral tissues and seed contained within are of immense importance in describing the fruits journey.
Genes controlling the encasing of ancestral maize (teosinte)
kernels in a strong fruitcase (derived from the glume) and
the adhering lemmae and palea tissues in hulled barley have
been identified (Wang et al., 2005; Taketa et al., 2008). The
hulled nature of the barley is quite unique in the cereals and
so identifying the gene, a member of the AP2-EREBP gene
family, controlling this feature will facilitate an understanding of why it has persisted (Taketa et al., 2008). There have
been extensive advances in identifying the genetic basis of the
shattering process since 2006, particularly in rice and more
recently in sorghum. Furthermore, in some intriguing cases,
the genes involved were related to those regulating fruit development and dehiscence in eudicots. Key shattering loci identified by QTL approaches in rice identified SH4 and qSH1,
which encode trihelix and homeodomain transcription factors, respectively (Konishi et al., 2006; Li et al., 2006). qSH1
is the orthologue of RPL (REPLUMLESS) in Arabidopsis.
Detailed analyses revealed that the genetic basis of qSH1
and RPL function in rice and Brassicaceae were analogous
(Arnaud et al., 2011) where the cis element that modified
qSH1 expression in rice was also affected in Brassica replums.
Map-based cloning of an introgressed shattering locus identified SHAT1 as a third component in rice shattering, defining the abscission layer (AZ) in the rice rachilla (Zhou et al.,
2012). SHAT1 is the orthologue of Arabidopsis AP2, a floral
identity gene in the ABC model, but more recently also shown
to have a role in negatively regulating RPL in replum development preventing overgrowth of the replum tissue in the carpel
(Ripoll et al., 2011). The major domestication locus in wheat,
Q, also encodes an AP2-like gene that contributes to various
domestication traits including rachilla fragility and grain size
(Simons et al., 2006). A YABBY family TF (YABBY2-like)
was identified as an important determinant of shattering in
sorghum, and also in rice and maize suggesting convergent
evolution (Lin et al., 2012). This gene has not been assigned
an explicit function in Arabidopsis, but its orthologue in
tomato had been identified as the basis of the fas locus controlling locule number and fruit size difference between wild
and cultivated tomato (Cong et al., 2008).
In terms of the specification of the grass carpel itself, initial
studies in rice found that, in contrast to eudicots, AG was not
the master controller of carpel identity in cereals; although
duplicated AG orthologues in grasses, and OsMADS3 and
OsMADS58 in rice, affect carpel development, they did not
specify the organ’s identity (Yamaguchi et al., 2006). This role
was assigned to the CRC orthologue DROOPING LEAF
(DL), where mutants produced stamens instead of carpels
(Nagasawa et al., 2003; Yamaguchi et al., 2004). More recent
studies, however, using a suite of insertion mutants, showed
that both AG orthologues redundantly controlled female
reproductive organ identity suggesting that AG-control of
carpel identity was indeed conserved in eudicots and monocots (Dreni et al., 2011). To date, rice remains the only monocot for which we have explicit functional data on all the C and
D class genes (Dreni and Kater, 2014).
Maize differs significantly from rice, wheat, and barley in
having separate male and female flowers. The male flowers
follow a developmental programme that represses growth of
a carpel, whereas in the female flowers the carpel develops
into characteristic corncobs or ears. The HD-ZIP gene, GT
(GRASSY TILLERS1), was identified in a screen for floral
development mutants in maize where the growth of carpels in
the male flower was derepressed in the gt1 mutant (Whipple
et al., 2011). The ability of GT1 to repress lateral growth
is manifested in the number of ears produced in the female
flowers (Wills et al., 2013) where it was identified as the
basis of the prol1.1 (prolificacy) locus where increased GT1
expression in maize compared with ancestral (and multipleear forming) teosinte suppressed the initiation of secondary
ear buds (Wills et al., 2013). Grain number increase in barley
domestication was associated with a transition from two-row
to six-row spikes. This transition was found to be controlled
by the VRS1 gene, which encodes a class 1 HD-ZIP TF that
acted in wild barley by suppressing the growth or lateral meristems (Komatsuda et al., 2007), and is also paralogue of GT1
(Whipple et al., 2011). A modifier of the 2-to-6 row transition,
intermedium-C, was identified and encodes the orthologue of
TB1 (TEOSINTE BRANCHED1; Ramsay et al., 2011), the
main determinant of apical dominance in cultivated maize
(Doebley et al., 1997).
Fewer master regulators specific to the development of the
grain (pericarp and seed within) have been identified (Sabelli
and Larkins, 2009). In cultivated cereals and most grasses, the
endosperm is the largest compartment in the harvested grain
and is differentiated into functionally distinct subdomains,
which can include the aleurone, modified aleurone or transfer
layer (at the junction of maternal vasculature and endosperm),
central starchy endosperm, and embryo-surrounding region
endosperm. The organization of the surrounding maternal
fruit and seed tissues varies, affecting the possible routes by
which sugars and amino acids are supplied to the developing
endosperm. For example, the generally accepted conduit for
maternal nutritional supplies in wheat grains is through the
nucellar projection and modified aleurone (Wang et al., 1995;
Fig. 4). Rice, however, also uses another pathway via the
nucellar epidermis (Oparka and Gates, 1981). OsMADS29
was recently shown to control nucellus degeneration in the
developing rice grain with reduced expression producing
shrunken seeds and reduced starch synthesis (Yin and Xue,
2012). Degeneration of the nucellus, and of the surrounding
maternal tissues generally, is an important accompaniment to
endosperm and embryo growth in cereal grains. This gene is
an orthologue of B-sister genes GOA and ABS (Table 1). This
4498 | Kourmpetli and Drea
Fig. 4. Triticum aestivum (bread wheat). Left; photograph of a spike, spikelet, and grain (Hands et al., 2012). Right; caryopsis/grain in longitudinal profile
and caryopsis/grain in transverse profile. A close-up of nucellar projection and adaxial endosperm is shown bottom right. Drawings based on Esau
(1960), Drea et al., (2005), and Krishnan and Dayanandan (2003).
analysis illustrates the interplay of maternal and filial tissues
in the grain’s development.
In later stages of grain development forward genetics approaches (mutant screens) identified genes such as
OPAQUE2 in maize as key regulators of storage protein gene
expression (Hartings et al., 1989), and several TFs from the
DOF, MYB, and BZIP gene families have been characterized in barley grains where they form complexes that regulate
storage protein genes and genes responding to GA (gibberellic acid) and ABA (abscisic acid) hormones important in
the maturation and germination process (Table 3). One of the
few genes shown to specify particular tissues early in the grain
development is ZmMRP1, a determinant of the endosperm
transfer layer in maize (Gomez et al., 2009; Table 3). Even
though different cereals have alternative transfer cells with
functional homology, these may not be genetically homologous tissues in the evolutionary sense as they lack an identifiable orthologue of the MYB single repeat ZmMRP1 gene
(Hands et al., 2012).
Much of the molecular genetic research in cereals such as
wheat has been hampered by the size and complexity of the
genome (Shewry, 2009). Rice has formed the main monocotyledonous model system in terms of genomic resources,
whereas maize provided an extensive resource and history
of developmental genetics. However, rice as a semi-aquatic
tropical species lacks many important temperate cereal traits.
But with the recent and rapid advances in barley and wheat
resources, including genome sequence (Brenchley et al., 2012;
IBGSC, 2012), the stage is set for an exciting era in temperate cereal research generally, and grain research specifically.
Before genome sequences became available for wheat and
barley, Brachypodium distachyon, had been developed as
a new model system for the temperate cereals (IBI, 2010).
Diploid B. distachyon offers one of the smallest genomes to
be found in the entire grass family along with many other
physical and phylogenetic attributes that make it suitable as
a temperate grass model (Mur et al., 2011; Opanowicz et al.,
2008). Logistically, the small stature, rapid life cycle, and
simple growing conditions are particularly useful features
for lab-based research where extensive or field-based growth
facilities may not be available. Also, there is huge intrinsic
value in having a wild uncultivated grass as a tractable model
in comparative and ecological studies (Hands and Drea,
2012; Mur et al., 2011).
The cereal grain as a nutritional powerhouse
Just as the BIA biosynthetic pathway of opium poppy has
been teased apart, the starch, cell wall, and protein metabolic
pathways in the grain that determine its uses/quality have
also been characterized in depth. ‘Whole grains’ retain the
remaining pericarp adhering to the seed (in the ‘bran’) and the
associated nutritional value in terms of increased fibre that
is usually removed in the ‘refined’ milling processes. Several
different types of storage protein and the occurrence and
relative amounts of these different proteins is an important
and distinctive feature of different species and an important
determinant of grain quality for bread-making etc. Amongst
the Triticeae species and maize the prolamins form the dominant protein class and are highly significant to the processing
and qualities of the grain, giving wheat flour is viscoelastic
properties (Gibbon and Larkins, 2005; Shewry and Halford,
Fruit development in poppy and cereals | 4499
2002). In oat and rice, globulins are the dominant storage
proteins, with prolamins forming only a minor component
of this fraction (Bewley and Black, 1994). In Brachypodium
globulins account for the majority of total extractable grain
protein, prolamins representing less than 12% (Larre et al.,
2010; Laudencia-Chingcuanco and Vensel, 2008).
The central endosperm of Brachypodium is relatively starchpoor; about 10% of total grain weight as opposed to 35–40%
in primitive wild wheats and 50–70% in domesticated cereals
(Guillon et al., 2011), and the starch granules are small, with
uniform size distribution and one or a few granules per plastid
in contrast to the bimodal distribution typical of the Triticeae
(Opanowicz et al., 2011). In grass endosperms the starch precursor, ADP–glucose, is also synthesised in the cytosol and
genes for components of its synthesis and transport into
plastids are unique to grasses (Comparot-Moss and Denyer,
2009). The alternate cytosolic pathway is dominant in both
wild and domesticated grains, which suggests an evolutionary
advantage; possibly that cytosolic production of ADP–glucose is energetically more efficient that plastidial starch synthesis. RSR1 is an AP2-like TF that was identified in rice as
being a negative regulator of starch synthesis genes in grains,
with mutants having bigger seeds (Fu and Xue, 2010). This is
one of the few examples of the identification of a specific TF
regulating an important metabolic pathway. In terms of starch
flux in the context of the grain, Radchuk et al. (2009) have
effectively described the dynamics of starch biosynthesis and
degradation in the context of the tissues of the fruit (pericarp)
and seed (maternal and filial tissues) in barley, which effectively links anatomy and biochemistry.
The Poaceae are distinctive for their deposits of
(1,3;1,4)-β-d-glucan (β-glucan) and comparative genomics
has played an important role in identifying the β-glucan synthase genes in grasses (Fincher, 2009). Glucose from hydrolysed β-glucan was shown to play a role in the sugar-recycling
mechanism during Zea mays seedling growth (Gibeaut and
Carpita, 1991) and suggests that β-glucan can function as a
readily convertible storage compound in addition to its structural role (Burton et al., 2010). Cell walls have major impacts
upon the nutritional quality and end use properties of cereal
grains and, as with storage proteins, the cell wall profiles in
grains are often distinctive to the genus, species, and even cultivar (Toole et al., 2012). In grains of the major domesticated
cereals the cell walls typically account for around 3–8% of the
total grain weight. Guillon et al. (2011) reported that the cell
wall polysaccharide content of dehulled Brachypodium grains
was 60%. With relatively little starch, it seems that much of
the carbohydrate material in the grain is contained within
the very thick cell walls of the endosperm (Guillon et al.,
2011; Opanowicz et al., 2011). This feature is distinctive when
compared with the grains of barley, wheat, maize, and rice,
characterized in detail to date (Hands et al., 2012). Trafford
et al. (2013) looked at the significance of the thick cell walls/
small cell size in relation to starch synthesis and presented a
model where failure of cell expansion in Brachypodium results
in continued β-glucan deposition in walls and is linked to the
downregulation of starch synthesis components and low
starch.
Conclusions
Cross-referencing Tables 1–3 and reviewing the research literature on comparative development shows that common
genes are involved in similar but different aspects of fruit/seed
development and maturation between eudicots and monocots, and that their roles are often modified in the context of
the new morphology and evolutionary distance. OsMADS29/
ABS (B-sister) affect the development of the maternal tissues
of the seed (nucellus and integuments) in rice and Arabidopsis
(Nesi et al., 2002; Yin and Xue, 2012) while affecting starch
accummulation in the grain. This link between central developmental regulators and commercial metabolic products
is also evident in the case of AP2 and SHP orthologues in
tomato, which affect the carotenoid accumulation in the ripening fruit (Chung et al., 2010; Vrebalov et al., 2009). Given
that seed dispersal in a fleshy fruit like tomato involves the
surrounding fruit tissues ripening and degrading, the role
of these genes in affecting the rate of ripening could also be
taken to constitute a role in fruit shattering/dehiscence and
seed dispersal as it is in Arabidopsis and rice (in the case of the
AP2 orthologue SHAT1; Zhou et al., 2012). AP2 is emerging
as a ubiquitous determinant of various aspects of fruit development in eudicots and grasses (Ripoll et al., 2011, Ohto
et al., 2009; Zhou et al., 2012, Simons et al., 2006; Houston
et al., 2013). An intriguing case of conservation in the regulation of the RPL gene and its functional significance in seed
dispersal has been demonstrated in Brassicaceae and rice
(Arnaud et al., 2011). As for our MADS-box Cs and Ds, they
will continue to be revisited many times and in many more
species (Heijmans et al., 2012), whereas the FUL genes have
already shown interesting diversification within Ranunculales
(Pabon-Mora et al., 2012; 2013). Current and future work
in cereals is already, and will continue to uncover patterns
of conservation and diversification of regulatory gene function; in the basal eudicots there is an exciting programme of
comparative fruit development in progress that promises to
reveal much about development in the fruit and other tissues
in this group of plants as well as extending what we know
about the function of these important genes across the angiosperms. Eventually what we know about the genes regulating
the fruits developmental programme from initiation though
harvesting may be joined more seamlessly.
Acknowledgements
The authors apologize for the huge volume of relevant research not cited in
this review owing to limited space. Drawings in Figures 3 and 4 were done by
Robert Harris based on cited work. Work on poppy and cereals in the lab is
funded by The Leverhulme Trust and BBSRC, respectively.
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