cell elimination as a developmental strategy in angiosperm seeds

12 Pages·2017·0.73 MB·English

Journal of Experimental Botany, Vol. 68, No. 4 pp. 785–796, 2017
doi:10.1093/jxb/erw364 Advance Access publication 4 October 2016
REVIEW PAPER
Dying to live: cell elimination as a developmental strategy in
angiosperm seeds
Gwyneth C. Ingram*
Laboratoire Reproduction et Développement des Plantes, Université de Lyon, CNRS (UMR 5667), INRA (UMR 0879), UCB Lyon 1,
Ecole Normale Supérieure de Lyon, F-69342 Lyon, France D
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* Correspondence: [email protected] lo
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Received 1 July 2016; Accepted 13 September 2016 fro
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Editor: Steve Penfield, John Innes Centre ttp
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Abstract e
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The complete elimination of unwanted cells during development is a repeated theme in both multicellular animals and .o
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in plants. In plants, such events have been extensively studied and reviewed in terms of their molecular regulation, of .c
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marker genes and proteins expressed, and in terms of cellular changes associated with their progression. This review m
will take a slightly different view of developmental cell elimination and will concentrate specifically on the numerous /jxb
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elimination events that occur during ovule and seed development (here grouped together as seed development). It rtic
asks why this cell elimination occurs in specific seed tissues, in order to understand something about the commonali- le
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ties underlying how seemingly disparate events are triggered and regulated. Finally, by placing the seed in its broader b
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evolutionary context, the question of why cell elimination may have emerged as such a key component of the seed tra
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developmental toolbox will be considered. t/6
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Key words: Cell death, degeneration, endosperm, embryo, seed, testa. /78
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What are seeds? by
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The sexual lifecycle of land plants comprises alternating mul- From this ‘primitive’ state, the evolution of the angiosperm es
ticellular haploid (gamete-forming, also known as gameto- seed required several major innovations. The first, which is t on
phyte) and multicellular diploid (spore-forming, also known thought to have occurred independently in several different 27
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as sporophyte) generations. Meiosis occurs within specific lineages during land plant evolution, was a transition from o
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sporophyte tissues (the sporangia), and gives rise to haploid homospory (where all spores and gametophytes are morpho- e
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spores. In so-called ‘ancestral’ land plants (such as the mosses), logically identical, and produce both male and female gam- be
these are released from the sporophyte and germinate to pro- etes), to heterospory. In heterosporous plants two distinct r 2
0
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duce independent multicellular gametophytes (green ‘leafy’ spore types, the megaspore (giving rise to the female game- 8
moss plants for example). Gametophytes ultimately generate tophyte, which in turn produces eggs) and the microspore
female and male (mobile) gametes (eggs and sperm), in struc- (giving rise to the male gametophyte which produces sperm)
tures called archegonia and antheridia respectively. Gametes are distinguished. Seed evolution then required the retention
meet and fuse to give rise to the next generation of diploid of megaspores, and the female gametophytes arising from
sporophytes (for example the stalked, capsule-forming struc- them, by the increasingly dominant and independent sporo-
tures seen on the surface of many mosses). In most ancestral phyte. Ultimately this led to the evolution of the ovule, com-
land plants, the sporophyte is nutritionally dependent upon posed of a protective organ (the integument) surrounding
the gametophyte. the megaspore-generating megasporangium (also known in
© The Author 2016. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved.
For permissions, please email: [email protected]
786 | Ingram
seed plants as the nucellus). These adaptations produced a
situation similar to that seen in modern-day gymnosperms.
These seed plants bear ‘naked’ ovules (borne in the axils of
leaf-derived organs) in which the nucellus and female game-
tophyte are enclosed by an integument (Linkies et al., 2010;
Endress, 2011; Pires, 2014). In many extant gymnosperms,
the female gametophyte absorbs nutrients from the maternal
sporophyte via the megasporangium, and proliferates to pro-
duce multiple egg-containing archegonia embedded within a
nutrient-storing tissue. Upon delivery of sperm cells by pol-
len grains (male gametophytes), multiple egg cells can be fer-
tilized, although generally only one embryo survives and any Fig. 1. Schematic representation of Arabidopsis seed development.
supernumerary embryos degenerate. The surviving embryo Tissues in which cell elimination occurs are labelled. (A) Developing ovule
prior to degeneration of the distal nucellus. The surviving megaspore is
grows invasively into the female gametophyte, absorbing
labelled (m). (B) Mature ovule. The egg cell is highlighted in purple and the D
nutrients, until seed maturity (recently reviewed in Cairney o
rest of the female gametophyte (g) is shown in grey. (C) Young fertilized w
and Pullman, 2007; Linkies et al., 2010). seed prior to cell elimination in the inner integument. The embryo proper nlo
Angiosperms are believed to have arisen from an ancestral is labelled (e). The position of the distal nucellus, which undergoes partial ad
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gymnosperm, and are thought to owe their success (includ- elimination after fertilization, is labelled (n). The position of the micropyle, d
ing an extremely rapid radiation), in part, to two further through which pollen tube ingress occurs, is shown by a green arrow in from
major reproductive innovations. The first is the production panels B and C. The ‘medial’ cell layer of the inner integument and its h
abaxial epidermis are shown in medium and dark blue respectively in ttp
oanf gfliooswpeerrsm. W oitvhuilne st haersee sfpuelclyia leiznecdlo rseepdr owduitchtiinv e ssptreucicatluizreesd, panels B and C. s://a
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organs called carpels. These play roles in pollen reception/ Ingram, 2010). The seed compartments must therefore interact d
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selection, ovule and seed protection, and seed dissemina- both physically and chemically, to allow successful seed devel- m
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tion (Scutt et al., 2006). Secondly, angiosperm seeds contain opment. In evolutionary terms, however, the two main inter- .o
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an endosperm. Pollen grains in angiosperms (and indeed in organismal interactions that occur in seeds arose well before p.c
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some gymnosperms) deliver two genetically identical sperm the emergence of the angiosperms. m
nuclei to ovules via the pollen tube. In angiosperms only The interactions involved in the retention and nourishment /jxb
one pollen tube is received by each ovule, but both sperm of the sporophytic embryo within the female gametophyte are /artic
nuclei fertilize female gametophyte derived cells; one fusing likely have the most ancient origins. The moss gametophyte le
with the egg cell to form the zygotic embryo, and the second supports, but does not fully enclose, the developing sporo- -ab
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with the central cell, which itself is formed by the fusion of phyte (Tanahashi et al., 2005). A similar situation is seen dur- tra
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two haploid gametophyte nuclei in many angiosperms. This ing the early development of the fern sporophyte, although t/6
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fusion of a sperm nucleus with the central cell generates the the latter rapidly becomes an independent organism. In the /4
endosperm. The endosperm plays a similar role to the gym- lycophyte Selaginella, sporophytic embryos grow invasively /78
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nosperm megagametophye-derived nutritive tissue, absorbing into a specialized gametophyte-derived nutritive tissue, and /2
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nutrients from the maternal sporophyte and then transferring then emerge in a process that looks deceptively like seed ger- 27
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them to the developing embryo either during seed develop- mination (Webster, 1967). A similar invasive growth into a 4
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ment or upon germination (Olsen, 2004; Li and Berger, 2012). nutrient storing tissue (female gametophye or endosperm) b
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Linking the initiation of nutrient storage in the endosperm to is observed during both gymnosperm and angiosperm seed gu
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fertilization in angiosperms may reduce waste when fertiliza- development (Cairney and Pullman, 2007; Yang et al., 2008). st o
tion does not occur (Baroux et al., 2002). In addition, fertili- The retention of the megaspore by the maternal sporo- n
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zation dependency is thought to provide a degree of paternal phyte and the subsequent extended interaction of maternal 7
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control over endosperm-mediated nutrient allocation to the tissues (the nucellus and integument) with the developing o
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developing embryo, generating parental conflict, which has female gametophyte occurred later in evolutionary terms m
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been proposed to strengthen reproductive barriers and drive (Linkies et al., 2010). This ultimate step in the conversion e
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speciation (Wolff et al., 2015; Pires et al., 2016; reviewed in of the female gametophyte from an autonomous plant to a 0
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Pires, 2014; Lafon-Placette and Kohler, 2016; Lafon-Placette ball of cells, totally dependent upon the maternal sporophyte 8
et al., 2016). for nutrition and protection, arose early during seed plant
In summary then, just after fertilization the angiosperm emergence, and presumably involved the setting up of novel
seed is composed of tissues from four genetically distinct com- communication pathways, enabling both co-ordinated devel-
ponents: the major tissues, the maternally-derived seed coat opment and regulated nutrient provision between the mater-
(integuments and nucellus), the endosperm and the embryo are nal plant and the nutrient-storing gametophyte.
organised one inside the other like Russian dolls (Fig. 1B). In Finally, specifically in angiosperms (and therefore much
addition, some un-fertilized cells of the haploid female game- later in evolutionary terms), the acquisition of fertilization
tophyte are usually present at this point. Nutrients are shuttled competence by the central cell of the female gametophyte led
to the endosperm and the embryo from the maternal tissues to a temporal synchronization of embryo development with
of the ovule, to drive seed and embryo growth (reviewed in female gametophyte-derived nutritive tissue (endosperm)
Cell elimination in angiosperm seeds | 787
proliferation. In addition to reproductive advantages, this elimination events occur in each of the three partners, and can
dramatic shift may well have imposed novel challenges and be observed both before and after fertilization. The different
constraints, necessitating mechanistic adjustments to existing tissues in which cell elimination occurs in the Arabidopsis seed
interactions within the developing seed. are shown in Fig. 1. In the maternal sporophyte, cell elimina-
tion occurs both within the nucellus (magasporangium) and
within the integuments (Fig. 1). After meiosis of the mega-
What is cell elimination? spore mother cell, the elimination of three of the four mega-
spores is observed in most angiosperm species, leaving only
Here I have deliberately chosen to classify cell death events
one living megaspore to undergo mitosis to form the (much
principally based on their outcome rather than upon the cel-
reduced) female gametophyte. Within this structure (which at
lular mechanisms through which they are achieved. I will thus
ovule maturity contains seven cells in Polygonum-type ovules,
make a distinction between the umbrella term ‘developmental
such as those of Arabidopsis), the descendants of only two
cell death’ and cell elimination. Developmental cell death events
cells (the egg cell and the central cell) survive, with the syn-
have been the subject of numerous reviews and classifications
ergid cells and the antipodal cells (Fig. 1B) being eliminated
based on the expression of specific types of proteins (and par- D
either during or relatively shortly after fertilization in most o
ticularly protease activities), classes of marker genes, or on the w
angiosperms. In the post-fertilization endosperm, elimination n
observation of particular events in the cytoplasm or nucleus events occur during embryo growth. Finally, the suspensor load
(such as DNA laddering and loss of membrane integrity, e.g. e
(Fig. 1C), an embryonic structure that supports early embryo d
van Doorn, 2011; Stael et al., 2014; Van Hautegem et al., 2014; development, is also eliminated during seed development in from
Olvera-Carrillo et al., 2015; Van Durme and Nowack, 2016). most angiosperms. h
Here I propose to divide the developmental cell death events ttp
Interestingly, although these cell elimination events have s
observed in the seed into two very broad categories. been documented to some extent in numerous species and ://a
The first is cell elimination, during which cell corpses are ca
appear to be an integral feature of developing seeds, in many d
(or appear to be) completely degraded and in which the space cases their regulation and function are poorly understood. In em
previously occupied by the dead cells is subsequently filled ic
addition, both their extent and developmental timing vary .o
by other tissues. This form of cell death is usually achieved up
widely across plants, suggesting that their regulation could be .c
though mechanisms that have been classified as ‘lytic’ cell o
an important target in the evolution of different seed devel- m
death, ‘autolytic’ cell death and ‘vacuolar’ cell death (van opmental strategies. /jxb
Doorn et al., 2011; Daneva et al., 2016). However, more exotic /a
processes, such as cell fusion, can also be classed under this rtic
Megaspore elimination le
umbrella term. Several cell elimination events in the seed have -a
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been largely ignored in the literature, and in this review I will s
As outlined above, in the majority of angiosperms, of the tra
therefore concentrate predominantly on recent advances in c
our understanding of where cell elimination occurs in seeds, fporuord umcee gaa spvoiarbelse pfreomdaulcee dg aamt emtoepiohsyitse, . oTnlhye oenliem siunravtiivoens otof t/68/4
of how it may be triggered, and of its contribution to the supernumerary megaspores appears to be spatially deter- /7
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developmental dynamics of the early developing seed. 5
mined, so that within a given species the surviving megaspore /2
The second is ‘structure-conserving’ cell death. During 6
usually occupies the same position within the nucellus [often 2
7
structure-conserving cell death the space originally occupied 4
the most chalazal (proximal) position (Fig. 1)]. However, 4
by a tissue remains occupied by recognisable cell corpses in between species, there is some variability in the position of 0 b
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some form. This process can occur through partial lysis (for the selected megaspore, and in some cases more than one gu
example where the cell protoplast is eliminated, but cell walls e
megaspore survives, suggesting that the selection of the s
remain intact), but also though cell death processes that have t o
functional megaspore may be a process that evolved inde- n
been termed ‘non-lytic’ or ‘necrotic’ (van Doorn et al., 2011; 2
pendently in different angiosperm lineages. Indeed, in some 7
Daneva et al., 2016). This form of cell death is usually associ- N
‘ancient’ angiosperm lineages, this selection does not occur, o
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ated with very specific functions in plants, for example the e
leaving up to four living megaspores which form megagame- m
formation of xylem elements, where the empty cells left by b
tophytes that physically ‘compete’ for access to pollen tubes, e
cell death are used as a conduit (Escamez and Tuominen, with selection only occurring at fertilization (Bachelier and r 20
2014). In seeds, structure-conserving cell death also occurs in 1
Friedman, 2011). However, it is not totally clear whether this 8
several tissues and plays important roles in seed physiology.
is an ancestral condition in angiosperms.
Although these events will be mentioned they will not be con-
Competition for nutrients may partly underlie the mecha-
sidered in detail in this review.
nism by which megaspore selection occurs in other angio-
sperm lineages, since the chalazal position is that closest to
Where does cell elimination occur in the the point where nutrients arrive in the nucellus. This idea is
supported to some extent by the finding that in Arabidopsis,
seed during development?
megaspore selection depends on chalazal cytokinin signal-
As can be seen above, seeds can be considered as the prod- ling (Cheng et al., 2013). Cytokinins are known to relay
ucts of a progressively evolving and increasingly intricate information regarding nutritional status in several contexts
cohabitation between three distinct plant generations. Cell (Glover et al., 2008). However, this is clearly not the whole
788 | Ingram
story because megaspore selection has systematically been in the synergids and thus to prevent the arrival of multi-
shown to coincide with active degradation of callose in the ple pollen tubes within the ovule (Hamamura et al., 2011;
cell walls of the viable megaspore (Rodkiewicz, 1970). The Maruyama et al., 2013). This second synergid has recently
presence/reinforcement of callose deposition in the walls of been shown to be eliminated through a highly original event
dying megaspore cell walls suggests an active isolation mech- involving fusion with the endosperm upon central-cell ferti-
anism that could cut off nutrient supplies or other signals lization (Maruyama et al., 2015). Subsequently ethylene pro-
from surrounding tissues. Although the molecular mecha- duced by the zygote upon egg cell fertilization is required for
nisms responsible for megaspore selection have not yet been the disorganisation of the synergid nucleus (Volz et al., 2013).
elucidated, in Arabidopsis the AGP18 arabinogalactan pro- The fate of the antipodal cells varies from species to spe-
tein has been shown both to be necessary for the initiation cies. In Arabidopsis, these cells degenerate either at or shortly
of female gametogenesis (Acosta-Garcia and Vielle-Calzada, after fertilization (Kagi et al., 2010; Song et al., 2014). This
2004) and to play a role in megaspore selection, since overex- degeneration is dependent upon endosperm-derived factors
pression of this protein results in the selection of several via- which have not yet been identified (Kagi et al., 2010). In con-
ble megaspores (Demesa-Arevalo and Vielle-Calzada, 2013). trast, in grasses such as maize, the antipodal cells prolifer-
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ate after fertilization and can become very numerous before o
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they ultimately die (Chettoor and Evans, 2015). The mech- n
Cell elimination in the female gametophyte lo
anisms involved in antipodal cell death are globally poorly ad
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The female gametophyte develops from the megaspore and, understood. d
in the Polygonum-type, contains eight nuclei enclosed in seven fro
m
cells; two synergids flanking the egg cell at the micropylar h
pole, the double haploid central cell, and the antipodal cells Nucellus cell elimination ttps
at the chalazal pole of the gametophyte (Fig. 1B). Of these, The nucellus (megasporangium) is a critical tissue in the devel- ://a
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all but the egg cell and the central cell will be eliminated at oping seed in that, as the source of the megaspore mother d
e
or soon after fertilization. The mechanisms controlling cell cell, it forms the interface between the zygotic and maternal m
ic
elimination events in this structure have almost exclusively compartments. In addition, it undergoes very dynamic devel- .o
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been studied in Arabidopsis and appear to be extremely opmental programmes in a number of species, and can reach p.c
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diverse. Although they have been recently and comprehen- an imposing size (e.g. in maize and Ricinus) before disap- m
sively reviewed (Kessler et al., 2010; Heydlauff and Gross- pearing almost completely by the end of seed development /jx
b
Hbea prdrot,v 2id0e1d4 ;h Veraen. Hautegem et al., 2014) a short update will ionf mthaen yn upclealnlutss. tIhna tc odfefeteer smeeindess fothre e xfianmalp slee,e dit siisz teh (eA glrvoews teht /article
Synergid cell elimination has been very extensively stud- al., 2016). In some plants, including some basal angiosperms -ab
s
ied due to its critical roles in the fertilization process. Of such as members of the Nymphaeales (Friedman et al., 2012; tra
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the two synergids, only one usually receives the pollen tube Friedman and Bachelier, 2013) as well as some monocots t/6
upon fertilization. The synergid cell death event that is trig- and Eudicots (including ‘quinoa (Chenopodium quinoa)’), the 8/4
gered by pollen tube reception is critical for fertility as it nucellus shares or even dominates the nutrient storage role of /7
8
5
appears to be necessary for pollen tube bursting and sperm the endosperm (Burrieza et al., 2014) by forming an alterna- /2
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cell delivery to the egg cell and central cell. In Arabidopsis, tive nourishing tissue, the perisperm, which can persist until 2
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the receptive synergid perceives the pollen tube via a signal- seed germination (Lopez-Fernandez and Maldonado, 2013a). 4
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ling pathway involving the FERONIA receptor-like kinase, The degeneration of the nucellus has been relatively widely b
y
the multispan membrane protein NORTIA and LORELEI, studied in a variety of different species. In Arabidopsis, the gu
e
a glycosylphosphatidylinositol-anchored protein (Escobar- majority of the distal nucellus (Fig. 1A) disappears during s
t o
Restrepo et al., 2007; Kessler et al., 2010; Liu et al., 2016). the growth of the female gametophyte, before fertilization n
2
This event is followed by synergid bursting and death which (Schneitz et al., 1995; Beeckman et al., 2000). Somewhat sur- 7
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involves FERONIA-dependent calcium signalling (Ngo prisingly, this process has not been characterized in any depth. o
v
e
et al., 2014). Synergid bursting additionally depends upon an However, the proximal nucellus persists through fertilization m
b
apparently independent pathway involving the activity of two before undergoing partial fertilization-dependent elimination. e
reproductive meristem (REM) family transcription factors This process has recently been shown to be negatively con- r 20
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VALKYRIE and VERDANDI (Mendes et al., 2016). These trolled by the FERTILIZATION INDEPENDENT SEED 8
in turn regulate the expression of other downstream factors (FIS) class of polycomb (PcG) proteins and by a member of
necessary for cell death including the mitochondrial matrix the B-sister clade of the MADs box transcription factor fam-
chaperone protein GFA2 (Christensen et al., 2002). Finally, ily, previously shown to be necessary for integument develop-
pollen tube discharge into the synergid has recently been ment, TRANSPARENT TESTA 16 (TT16) (Nesi et al., 2002;
shown to participate in the later stages of synergid degen- Xu et al., 2016).
eration suggesting that components of the pollen cytoplasm Although the nucellus is juxtaposed to the antipodal cells
post-rupture could be implicated in this process (Leydon of the female gametophyte prior to fertilization, the rela-
et al., 2015) tive chronology of cell elimination events occurring in these
Elimination of the remaining synergid is proposed to lead two cell types has not been simultaneously studied, and
to a rapid dilution of the pollen tube attractant produced their potential commonalities have not been addressed. It is
Cell elimination in angiosperm seeds | 789
however interesting to note that mutants with defective nucel- the placenta-chalazal region of the seeds of maize and some
lus elimination in Arabidopsis also show defects in the devel- other cereals undergoes a cell death event that involves early
opment of the chalazal endosperm (Xu et al., 2016). enucleation and loss of cytoplasmic contents, but again
The partial cell elimination described in the Arabidopsis maintenance of cellular structure. This event has been impli-
nucellus is a gradual process leading to a complete loss of cated in facilitating transport of nutrients unloaded from the
cell structure (Xu et al., 2016). It can be considered to resem- phloem to the endosperm (Kladnik et al., 2004).
ble autophagic or ‘recycling’ cell death in animals (for recent
comparative reviews of developmental cell death processes
Cell elimination in the integuments.
in plants see: van Doorn, 2011; Van Hautegem et al., 2014;
Olvera-Carrillo et al., 2015; Van Durme and Nowack, 2016), In the mature, desiccated Arabidopsis seed the only living
and indeed involves the expression of autophagy markers (Xu tissues are the residual endosperm and the embryo. All the
et al., 2016). Nucellus cell death in many other plant species cells of the maternal seed coat must therefore die during seed
appears to occur via a similar gradual process of degenera- development. However, these cell death events occur at very
tion and absorption (Dominguez et al., 2001; Hiratsuka et al., different times, and comprise both potential cell elimina-
D
2002; Greenwood et al., 2005; Chen et al., 2015a). In rice, this tion events and events in which cell structure is conserved. o
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process has been shown to be controlled by a B-sister MADS- The seed coat has multiple functions (recently reviewed in n
lo
box transcription factor closely related to TT16, OsMADS29 Radchuk and Borisjuk, 2014). In Arabidopsis, and likely in ad
e
(YaAn gr eectu arlr.i,n 2g0 1t2h;e Ymien ainn dn Xucueell,u 2s0 1d2e)g.radation is a link to mtoa tnhye oenthdeors pspeermcie as,n idt eamctbs rayso aa fctoern dpuhilto, epmro uvnidloinagd innugt irnie tnhtes d from
endosperm growth and differentiation. Nucellus elimination chalazal zone of the seed coat. This function is mediated by h
appears to be both necessary for (Radchuk et al., 2006; Yin transporters expressed both in the chalazal seed coat and the ttps
and Xue, 2012) and dependent upon (Radchuk et al., 2011; integuments that permit the movement of nutrients across ://a
c
a
Xu et al., 2016) endosperm development. In Arabidopsis it symplastic boundaries and ultimately into the endosperm d
e
has been shown that the endosperm-specific MADS protein cavity (e.g. Tegeder et al., 1999, 2000; Ladwig et al., 2012; m
ic
AGL62, which is expressed post-fertilization, is necessary for Chen et al., 2015b; Sosso et al., 2015). In addition, the seed .o
u
the breakdown of nucellar tissues, indicating the presence of coat physically constrains the growth of the seed, in a process p.c
o
a mobile ‘signal’, the identity of which is unknown (Xu et al., that involves active responses to physical cues (stretching) m
2016). Since AGL62 is absolutely required for endosperm imposed by the developing endosperm (Creff et al., 2015). /jxb
grerloawtet hto ( Kgraonwgt eht- raell.a, t2e0d0 8ch),a int gise sp oins seibnldeo tshpaetr tmh es isnigkn satlr ecnogutlhd Bupoothn ocfe ltlh veisaeb ‘ieliatyr,ly n’ efcuenscstiitoantisn gin a t hceo -soereddi ncoataito anr eb edtewpeeennd tehnet /article
(leading to changes in nutrient status in the nucellus), or onset of seed coat cell death and embryo-endosperm devel- -ab
s
could even be triggered by mechanical stress caused by the opment. How this co-ordination is achieved remains unclear, tra
c
growth of the endosperm within the confines of the mater- although it has been shown that early integument senescence t/6
nal seed coat. Another possibility is that the signal could is prevented both by polycomb group proteins and by an 8/4
be hormonal. In rice, nucellar expression of OsMADS29 is AGL62-dependent signal from the fertilized endosperm in /78
5
stimulated by auxin, and endosperm growth has been linked Arabidopsis (Roszak and Kohler, 2011). /2
6
to auxin production in a range of different systems includ- In Arabidopsis, the outer integument is composed of only 27
4
ing Arabidopsis, Medicago and maize (Lur and Setter, 1993; two epidermal cell layers, while the inner integument has an 4
0
Forestan et al., 2010; Bernardi et al., 2012; Figueiredo et al., internal (third) cell layer in more proximal regions (Beeckman by
2015; Noguero et al., 2015). Furthermore, auxin has been et al., 2000) (Fig. 1). The two integument cell layers that can gu
e
shown to move out of the endosperm and into maternal tis- be considered to be ‘eliminated’ during seed development in st o
sues during seed development in species such as Fragaria Arabidopsis are the ‘medial’ cell layer of the inner integument n
2
vesca (Kang et al., 2013). Another candidate hormone is eth- and its abaxial epidermis. This process is progressive, initiat- 7 N
ylene, the production of which in the endosperm has been ing at around the heart/early torpedo stage in embryo devel- o
v
e
shown to be involved in nucellus degradation in the cucurbit opment and continuing as the embryo expands (Nakaune m
b
Sechium edule (Lombardi et al., 2012). et al., 2005). Cell death in these tissues again occurs through e
In addition to cell elimination, a second type of cell death an apparently lytic process, and ultimately the cell corpses are r 20
1
has been observed in the nucellus of plants that use the nucel- impossible to distinguish from neighbouring cells, although 8
lus as a long-term nutrient storage tissue or perisperm. This some cell wall material may remain. As in many plant cell
has been best studied in quinoa where starch deposition in death processes, the activity of caspase-like enzymes (in this
perisperm cells occurs concomitantly with a cell death pro- case the cysteine protease DELTA-VPE) has been associ-
cess in which cell structure is maintained and which strongly ated with cell elimination in the integuments (Nakaune et al.,
resembles that observed in the starch endosperm of cereals 2005), but the trigger for cell death remains unclear. One
(Lopez-Fernandez and Maldonado, 2013a; Burrieza et al., possibility is that embryo growth imposes a physical strain
2014). This type of cell death appears to be rather unique on the testa, which triggers cell death events. The idea that
to seed nutrient-storing tissues (van Doorn, 2011). As in the cell death could be a consequence of physical factors associ-
cereal endosperm, tissue elimination and nutrient hydroly- ated with the growth of filial tissues has also been invoked
sis in this tissue occur only upon seed germination. Finally, in cereals (Radchuk et al., 2011). However, this possibility
790 | Ingram
has not yet been investigated in depth. Loss of function of that at least two different types of endosperm cell death
two NAC domain transcription factors expressed in the outer occur during seed development. The first, which has been
integument, NARS1 and NARS2, has been shown to retard widely studied because of its importance in the stabilization
cell death in the inner integument in Arabidopsis, although of storage compounds such as starch, is that observed in the
the underlying mechanism for this phenomenon is unclear persistent endosperm of cereals. This cell death process is a
(Kunieda et al., 2008). ‘structure conserving’ cell death event that has been recently
From early in development, the cell walls of the develop- and extensively reviewed (Dominguez and Cejudo, 2014;
ing seed coat are highly modified both through thickening Lopez-Fernandez and Maldonado, 2015) and therefore will
(to impart mechanical strength) and the deposition of both not be considered in depth in this review.
suberin (Espelie et al., 1980; Beisson et al., 2007; Vishwanath In cereals, as in other angiosperms, cell elimination events
et al., 2013) and cutin (Van Lammeren et al., 2006; De Giorgi also occur in the endosperm. This elimination occurs in the
et al., 2015) polymers that reduce the permeability of the seed endosperm immediately juxtaposing the developing embryo
coat. In addition, in Arabidopsis the seed coat accumulates and progresses as the embryo grows. In cereals, such as
proanthocyanidins that have been proposed to play protec- maize, this cell elimination has been very poorly character-
D
tive roles. The cell layers responsible for these modifications ized. However, a recent study clearly showed the presence o
w
in Arabidopsis are thought to be the endothelium [adaxial of nuclear DNA fragmentation, specifically in the embryo n
lo
epidermis of the inner integument, proanthocyanidin accu- surrounding endosperm in young barley kernels, but not in ad
e
mthueslaist io(Dn e( BGaiuodrgryi eett  aall..,, 22001054))] aanndd tphoet eandtaiaxlilayl ceuptiidne rbmioissy onf- epmorbtrinygo st hoer idoethae trh aetn dceolslsp earrme locestll sfr o(Tmra tnh ise tr eagl.i,o n2.0 1S4im), ilsaurply- d from
the outer integument [suberin biosynthesis (Beisson et al., in maize, a specific zone of endosperm cells that surrounds h
ttp
2007)]. These two cell layers, together with the highly special- the early developing embryo, the embryo surrounding region s
ized mucilage-producing outer cell layer, die late in seed devel- (ESR), is known to be eliminated during early seed develop- ://a
c
a
opment (Windsor et al., 2000; Andeme Ondzighi et al., 2008), ment, although the mechanisms behind this elimination are d
e
although there is some disagreement in the literature regarding poorly understood (Cossegal et al., 2007). m
ic
when exactly these various cell death events occur. These cell Dicotyledonous plants generally undergo a much more .o
u
p
death events can be classified as ‘structure conserving’, and the dramatic endosperm elimination during seed development. .c
o
protective roles of the cell walls left after these cell death events Interestingly, a beautiful cytological study in the endosperm m
are important for seed viability. Similar gradual but apparently of Solanum nigrum showed modification of the cell walls sur- /jxb
organized cell wall modification and cell death in the maternal rounding endosperm cells in a zone around the embryo prior /artic
seed tissues has been reported in a wide variety of species (e.g. to endosperm cell elimination (Briggs, 1993). Endosperm le
Van Lammeren et al., 2006; Radchuk et al., 2011; Lima et al., cells were found to separate, with extracellular material being -ab
s
2015) but again the triggers have not been investigated. secreted. These cells were then compressed as the embryo grew. tra
c
These observations suggest that cell wall modifications could t/6
8
Cell elimination in the developing endosperm precede elimination of the embryo surrounding endosperm in /4
the Solanaceae. Similar modifications to cell walls have been /78
5
The endosperm is the product of fertilization of the central observed during cell elimination in the endosperm of quinoa, /2
6
cell of the female gametophyte. It plays a key role in the devel- although the chronology of events in this species is less clear 27
4
opment of the seed both in nutritive terms (ferrying nutrients (Lopez-Fernandez and Maldonado, 2013b). 4
0
to the developing embryo from maternal tissues), but also in The observation that cell wall modification could be involved b
y
terms of seed growth (Costa et al., 2004; Berger et al., 2006; as an upstream factor in (rather than a consequence of) cell gu
e
Becraft and Gutierrez-Marcos, 2012; Li and Berger, 2012). elimination is particularly pertinent in light of a more recent st o
Unlike the situation in the seeds of Caffea, quinoa and, to a study investigating the mode of function of the endosperm n
2
lesser extent, cereals and grasses, where nucellar development specific basic-helix-loop-helix (bHLH) transcription factor 7
N
contributes to seed growth and in some cases determines the ZHOUPI/RETARDED GROWTH OF EMBRYO1 (ZOU/ o
v
e
final size of the seed, in many species it is predominantly RGE1) in Arabidopsis. Arabidopsis endosperm is almost com- m
b
endosperm expansion that drives seed growth. This is notably pletely eliminated during wild-type seed development, leaving e
the case in Arabidopsis, and in legumes such as peas. Despite only a single layer of specialized endosperm cells in mature r 20
1
this important growth-promoting role, the endosperm in seeds. Loss of ZOU function leads to an apparently complete 8
many species is a transient structure, all but disappearing by loss of endosperm elimination, giving mature seeds that con-
the end of seed development, and this dynamic and short life tain a large volume of persistent endosperm, and a severely
necessitates the co-ordinated elimination of the majority of stunted (but nonetheless viable) embryo (Kondou et al., 2008;
the endosperm cells. Again, this is the case in Arabidopsis. Yang et al., 2008). Although zou mutant endosperms do not
However, in other plants, including many monocotyledonous express the pre cell-death marker genes usually expressed in the
species, the majority of the endosperm is used as a persistent wild-type endosperm, these do not appear to be the direct (or
storage tissue, only being broken down and assimilated by the early indirect) transcriptional targets of ZOU activity, most of
embryo upon seed germination. which are annotated as encoding cell wall modifying enzymes,
As mentioned above, the study of cell elimination in the and are expressed well before pre cell-death markers in the
endosperm has been rendered more complicated by the fact wild-type endosperm (Xing et al., 2013; Denay et al., 2014;
Cell elimination in angiosperm seeds | 791
Fourquin et al., 2016). Consistent with the idea that ZOU The elimination of the suspensor
does not directly trigger cell death events, its ectopic expres-
Although some reports have suggested that cell death-asso-
sion does not trigger cell death in extra-embryonic tissues
ciated events (such as DNA fragmentation) could occur in
(Kondou et al., 2008; Yang et al., 2008). ZOU activity in the
multiple embryonic tissues, (Giuliani et al., 2002), there is
seed depends upon hetero-dimerization with the INDUCER
little evidence for such events leading to cell elimination in
OF CBP EXPRESSION 1 (ICE1)/SCREAM protein (Denay
any tissue but the suspensor. The suspensor is a structure that
et al., 2014), and it could therefore be argued that lack of cell
differentiates from the basal progeny of early cell divisions in
death upon ectopic expression of ZOU is due to lack of ICE1.
the zygote. It has been proposed to play important nutritive
However, ICE1 is relatively widely expressed during vegetative
roles, as well as to physically anchor the embryo within the
development, particularly in the stomatal lineage (Kanaoka
endosperm cavity (Kawashima and Goldberg, 2010; Endo,
et al., 2008), suggesting that ZOU-ICE1 heterodimers do not
2012). In addition, the suspensor appears to play impor-
directly induce cell death. Cytological studies of the wild-
tant embryonic patterning roles, notably through mediation
type Arabidopsis endosperm show that cells tend to ‘round
of basipetal auxin fluxes during very early embryogenesis
up’ during development, consistent with some degree of cell
(most recently reviewed in Jeong et al., 2016). The role of D
separation. This is not observed in the endosperm of zou o
the suspensor in patterning the embryo has been particularly w
mutants, which in addition shows an abnormal maintenance n
of arabinan epitopes (often associated with pectins, Willats thoroughly studied during somatic embryogenesis in Picea load
abies (a gymnosperm) where, intriguingly, a timely and well e
eInt taelr.e, s1ti9n9g8l)y ,i nzo eun mdoustpaenrtms s hceolwl w aanl las b(nFoorumrqaulliyn heitg ha lp., r2es0s1u6r)e. co-ordinated, lytic suspensor cell death involving autophagic d from
within the zygotic compartment at the torpedo stage of devel- processes and the activity of cysteine proteases of the meta- h
caspase family appears to be critical for embryonic pattern- ttp
opment when the embryo is expanding rapidly, suggesting s
that the embryo and the endosperm compete for space within ing (Suarez et al., 2004; Minina et al., 2013; Smertenko and ://a
c
Bozhkov, 2014). In contrast, a developmental role for suspen- a
the seed coat of these mutants (Creff et al., 2015; Fourquin d
et al., 2016). Based on these results it has been suggested that sor cell death in angiosperms is less well established, since em
endosperm elimination could require cell wall modification plants showing retarded suspensor elimination, for example ic.o
due to loss of function of the cell-death inducing peptide up
of the endosperm that might predispose endosperm to crush- .c
KISS OF DEATH have not been reported to have notable o
ing/bursting upon embryo growth. In support of this model, m
in mutants where endosperm development occurs normally embryonic phenotypes (Blanvillain et al., 2011). /jxb
but embryo growth is impaired, the endosperm is not elimi- quIinnotear es(Ltinogpleyz, -aFte rlenaasnt dinez m aanizde M(Garlidmoanualdt oe,t a2l0.,1 32b0)1,5 )t haenrde /artic
nated, despite the expression of ZOU and direct ZOU targets. le
Endosperm elimination would thus appear to be depend- appears to be a clear temporal link between the onset of sus- -ab
ent upon embryo growth, although a role for an additional pensor loss and the elimination of the endosperm surround- stra
ing the developing embryo. In quinoa, the cellular changes c
embryo-derived signal not produced in these early embryo- t/6
associated with the two processes also appear to be very 8
lethal mutants cannot yet be formally excluded. Nonetheless, /4
unlike the situation in the persistant endosperms of zou similar. This could suggest either that the two processes are /78
triggered by the same signals, or that one cell death event 5
mutants, the ‘persistent’ endosperms of seeds with defective /2
embryos express pre cell-death markers apparently normally, could depend upon/be triggered by the other. This last con- 627
sideration brings up an important and, to date, unaddressed 4
suggesting that the activity of ZOU in modifying cell walls 4
0
predisposes endosperm cells to die, even if it is insufficient for point. Many researchers have concentrated upon trying to b
y
their total elimination (Fourquin et al., 2016). understand how cell death events in the seeds are initiated. gu
However, in light of the proximity of the various seed tis- e
ZOU is a unique and ancient member of the bHLH fam- sues, it may be just as pertinent to ask how cell death events st o
ily in plants, and is conserved in gymnosperms and even n
are prevented from spreading once they have been initiated. 2
in lycophytes, suggesting that its ancestral role may mas- 7
This is true not only with regard to the embryo, which is sur- N
sively predate its developmental function in the angiosperm o
v
rounded by a dying endosperm (and in many cases attached e
endosperm (Yang et al., 2008). It is perhaps unsurprising then m
to a dying suspensor), but also within the endosperm, where b
that the function of ZOU appears to be at least partially con- e
some cells die, but other remain living, and in other adjoining r 2
served in maize, where RNAi of the ZmZOU gene leads to a 0
persistence of the ESR, and a slight decrease in embryo size tissues. In light of this, the recent observation that suspensor 18
death in tobacco appears to be regulated by a fine balance
(Grimault et al., 2015). Although this phenotype is not as dra-
between pro-death and anti-death factors (Zhao et al., 2013)
matic as that on zou mutants, it should be noted that the lines
is intriguing, and suggests that control of cell elimination
used in this study were not full knockouts. Furthermore, as
may be a highly complex balancing act in some tissues.
in Arabidopsis, ZmZOU interacts with members of the ICE1
bHLH family (Denay et al., 2014; Grimault et al., 2015).
Genetic evidence in Arabidopsis from complementation stud-
Inter-compartmental antagonism during seed cell
ies (Grimault et al., 2015) and the analysis of a hypermorphic
elimination
variant of ICE1 (Denay et al., 2014) suggests that it could be
ICE1, rather than ZOU that acts as the limiting factor in the Due to the fact that seed compartments are arranged one
heterodimeric complex during endosperm degradation. inside another, their development is irrevocably linked, both
792 | Ingram
at the physical and at the nutritional level. As a result, growth view of the situation. The direct and early targets of the ZOU
and development of one compartment will have unavoid- protein responsible for endosperm elimination in Arabidopsis
able consequences for surrounding compartments. Although do appear to predominantly be involved in cell wall modifica-
antagonistic development of adjacent seed compartments is tions (Denay et al., 2014; Fourquin et al., 2016). However,
not a new idea, recent publications discussed in the sections it has been shown that the OsMADS29 protein required for
above have brought it to the forefront of seed developmental nucellus degradation in rice directly binds to the promoters
studies. Notably, Xu et al. (2016) have shown convincingly of cysteine protease and nucleotide binding site-Leu-rich
that nucellus development and endosperm development repeat protein-encoding genes, which could directly trigger
are antagonistic processes so that, at least in Arabidopsis, cell death (Yin and Xue, 2012). Nonetheless, global transcrip-
if nucellus breakdown is impaired this can have an impact tional analyses of genes regulated by neither OsMADS29 nor
on the development of the endosperm, whereas normal TT16 have not yet been undertaken, and ectopic expression
endosperm development is required for nucellus breakdown. of TT16 has not been reported to cause ectopic cell death
The dependence of normal endosperm development upon (Nesi et al., 2002). A role for cell wall modification in nucellus
nucellus breakdown has also been demonstrated in rice (Yin elimination cannot therefore be eliminated.
D
and Xue, 2012; Nayar et al., 2013). Similarly, Fourquin et al. Cell wall modifications also occur during megaspore cell o
w
(2016) have demonstrated an apparent antagonism between elimination events, where the selection of the surviving meg- n
lo
embryo and endosperm development in Arabidopsis. Thus if aspore is correlated with a loss of callose from cell walls. ad
e
the endosperm does not break down, embryo growth is physi- Conversely, callose accumulation appears to be maintained/ d
cally impeded by the endosperm. Conversely, endosperm cells reinforced in the walls of megaspores destined for elimination from
are not eliminated if the embryo does not grow, or at least (Rodkiewicz, 1970; Zhou et al., 2016). This callose accumula- h
ttp
reach a certain developmental stage necessary for signal- tion is indicative not only of changes in the apoplastic con- s
ling to the endosperm. It is very tempting to draw parallels nectivity of megaspores with surrounding cells, but also could ://a
c
a
between these two antagonistic processes. However, although play roles in gating symplastic contacts (e.g. Vaten et al., 2011; d
e
in the latter example a physical antagonism between the Slewinski et al., 2012; Benitez-Alfonso et al., 2013; Maule m
ic
embryo and the endosperm clearly plays an important role et al., 2013), and is therefore likely to profoundly impact .o
u
p
in the phenomena observed, the mechanism underlying the the movement of nutrients. This, combined with the rapid .c
o
nucellus/endosperm relationship is not yet clear. expansion of the surviving megaspore (its conversion into an m
Whether further similar antagonistic relationships exist increasingly strong ‘sink’ tissue), could starve the remaining /jxb
remains to be investigated in more detail. Megaspore selec- megaspores, bringing up a second important point. /artic
tion, for example, appears to involve antagonistic interactions. le
Similarly, the development of the seed coat and the integu- Nutrient status sensing and cell elimination -ab
ments show some antagonistic aspects. However, although Plant cells are known to react to nutrient deprivation stra
one mutant defective in cell elimination in the seed coat also by undergoing ‘recycling’ cell death/senescence events ct/6
shows defective endosperm development (Kunieda et al., (Masclaux-Daubresse et al., 2010; Thomas, 2013; Balazadeh 8/4
2008), this has not been described for other mutants affected et al., 2014). The regulation of these events is impacted by a /78
in the same process (Nakaune et al., 2005). Furthermore, the wide variety of endogenous and environmental signals (e.g. 5/2
6
dependence of integument cell layer elimination upon the Baena-Gonzalez and Sheen, 2008; Gully et al., 2015; Meng 27
development of the zygotic compartment remains formally et al., 2016). It is possible that such starvation responses 44
0
undemonstrated, even though compelling correlations have could have been hijacked to facilitate cell elimination events b
y
been noted (Radchuk and Borisjuk, 2014). in the seed. gu
relUatniodnesrhstiapns dbientgw ethene bseaesdis cfoomr pthaert mapepnatsr ecnotulyl da nptraogvoidnei satinc ionS.e eFdo tri sesuxaesm tpenled, tion dAevrealboipd oinp sai sh ipgohslyt- afesrytnilcizhartoinoonu, si nfaitsiha-l est on
important basis for understanding the triggers underlying cell seed growth is driven by the endosperm, suggesting that this 27
N
elimination in the future. Two specific features deserve to be is the major sink tissue in the seed during early expansion. o
v
discussed in this light: cell wall modification and alterations Subsequently, embryo growth initiates and progresses with em
in nutritional relationships. astonishing rapidity, presumably causing a dramatic switch be
in the nutrient status of the endosperm from sink to source r 2
0
1
Cell wall modifications and cell elimination (or at least conduit). These changes are accompanied by dra- 8
Cell wall modifications underlie several of the cell elimina- matically changing patterns of nutrient transporter expres-
tion events that occur in developing seeds. This has been sion within both zygotic and maternal tissues (e.g. Chen
clearly demonstrated during endosperm cell elimination in et al., 2015b; Muller et al., 2015). Although the mechanisms
Arabidopsis and in Solanum, where cell wall modifications underlying these apparently sudden switches in sink identity
precede cell elimination during embryo expansion. (Briggs, remain unclear, and probably involve complex feedbacks,
1993; Fourquin et al., 2016). Controlled cell wall modifica- they are likely to lead to dramatic changes in nutrient status
tion provides a simple mechanism to explain changes in the within individual seed tissues at specific developmental time-
physical relationships between adjacent tissues that could points. Such changes could act as an important factor in pre-
underlie cell elimination events triggered by mechanically disposing specific cell populations to elimination. Although
induced stress. However, this may well be an over-simplistic such mechanisms would provide an attractive explanation for
Cell elimination in angiosperm seeds | 793
compartmental antagonism during seed development, it will Interestingly, the OsMADS29/TT16 clade of B-sister
only be by combining detailed, compartment specific metab- MADS box proteins also predates the angiosperms, but
olomics approaches with developmental studies that their is thought to have arisen well after ZOU, probably in an
importance can begin to be addressed. ancestral gymnosperm before the divergence of the gymno-
sperms and angiosperms (Becker et al., 2002). Genes in this
clade are mainly associated with female reproductive devel-
Developing a death wish: the evolutionary opment and differentiation, consistent with an ancestral
recruitment of cell elimination as a role for this family of proteins in the early seed, potentially
developmental mechanism associated with the retention of the female gametophyte by
the maternal sporophyte. Elucidation of the mechanisms
Several known cell-death regulating transcription factors through which TT16/OsMADS29 facilitate nucellus degen-
identified in non-seed developmental cell death processes eration and the degeneration of other tissues (in the case of
have been shown to cause cell death upon ectopic expres- OsMADS29), will allow a more direct comparison of the
sion, suggesting they directly activate cell death effectors mechanistic similarities between the cell elimination mod-
D
(such as metacaspases) triggering cell death. For example, ules acting downstream of ZOU and TT16/OsMADS29. o
w
the VASCULAR-RELATED NAC-DOMAIN6 (VND6) This could be very instructive in revealing how two totally n
lo
and VND7 proteins can induce xylem differentiation, includ- different classes of transcription factors have come to ad
e
ing cell death, upon induced ectopic expression, (Yamaguchi regulate two such apparently similar events during seed d
et al., 2010, 2011), as can the related SOMBRERO tran- evolution. from
scription factor, which plays a role in root cap differentia- In conclusion, a wide range of cell elimination events h
tion (Bennett et al., 2010). Whether the NARS1 and NARS2 occurs during the development of angiosperm seeds. Many ttps
NAC-domain transcription factors, implicated in integument of these appear to be controlled by a combination of differ- ://a
c
cell death (Kunieda et al., 2008), are also direct cell death entiation-associated priming and interactions, either physical ad
e
regulators remains to be tested. However, a repeated theme or chemical, between neighbouring seed compartments or m
ic
in the work reviewed above is that cell elimination in seeds with the male gametophyte. Despite their apparent similari- .o
u
is often controlled by the activity of seed-specific transcrip- ties in terms of outcomes (often lytic cell death events asso- p.c
o
tion factors, or transcription factor complexes, the ectopic ciated with highly regulated protease activities), these events m
expression of which is not, in itself, sufficient to induce cell are diverse in terms of the molecular control of their priming, /jxb
doef attihss.u Ien setnevaidro tnhmeseen ptrso ptreiimnse dse feomr ctoel lp erolimmointaet tihoen pervoednutsc ttihoant liinkterliyc arteefl reecltaitniogn tshhei psse qbueetwnteieanl etvhoe lvuetrioyn dairffye reesntatb cloismhmpoennet notfs /article
are additionally dependent upon the normal development of of the angiosperm seed. Further research into the precise cell -ab
s
other cells and/or tissues. This ‘priming’ is illustrated well in death triggers in each case will be required to establish how tra
c
the case of the REM transcription factors VERNANDI and these different pathways converge. t/6
VALKYRIE, the activities of which during ovule differentia- 8/4
tion do not, in themselves trigger cell death, but appear to /7
8
5
sensitise synergid cells to pollen perception via the FERONIA References /2
6
pathway (Mendes et al., 2016). 2
7
Acosta-Garcia G, Vielle-Calzada JP. 2004. A classical arabinogalactan 4
In the case of Arabidopsis endosperm elimination, ZOU 4
protein is essential for the initiation of female gametogenesis in 0
expression and ZOU-dependent cell wall modifications in the Arabidopsis. Plant Cell 16, 2614–2628. by
endosperm occur in the absence of embryo growth, but are Alves LC, Magalhaes DM, Labate MT, Guidetti-Gonzalez S, Labate gu
e
not sufficient to efficiently trigger cell death in these condi- CA, Domingues DS, Sera T, Vieira LG, Pereira LF. 2016. Differentially s
accumulated proteins in Coffea arabica seeds during perisperm tissue t o
tions, or upon ectopic expression (Yang et al., 2008; Grimault n
development and their relationship to coffee grain size. Journal of 2
et al., 2015; Fourquin et al., 2016). Thus ZOU expression in Agricultural and Food Chemistry 64, 1635–1647. 7 N
the endosperm appears to pave the way for endosperm elimi- Andeme Ondzighi C, Christopher DA, Cho EJ, Chang SC, Staehelin o
v
nation in a process dependent upon the growing embryo. LA. 2008. Arabidopsis protein disulfide isomerase-5 inhibits cysteine em
proteases during trafficking to vacuoles before programmed cell death of b
As mentioned in the introduction, the embryo-gametophyte e
(endosperm) interaction is probably the most ancient within tBhaec ehnedloietrh eJlBiu,m F rinie ddemvealonp WingE .s 2e0e1d1s.. PFelamnta lCe eglla 2m0e, t2e2 c0o5m–2p2e2ti0tio.n in an r 201
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unique transcription factor, having arisen before the diver- Sciences, USA 108, 12360–12365.
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(Yang et al., 2008; Grimault et al., 2015). Although studies in
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that the ‘endosperm elimination function’ may have evolved transcriptomic and metabolomic consequences. Journal of Experimental
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patterning. Developmental Cell 26, 136–147. Dominguez F, Moreno J, Cejudo FJ. 2001. The nucellus degenerates o
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BWeilnlenmetste Tn, vVa, nS ndeeln B T, oSocrhne Are, sS aBn. c2h0e1z0-. PSeOrMezB GRFE,R COa, mBEpAilhRoS KAI,N 1, and bgrya ain p dreovceelsosp mofe pnrto. gPrlaamntma e2d1 3c,e 3ll 5d2e–a3th6 0d.uring the early stages of wheat nloa
d
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