Flowering plants display a large spectrum of seed architectures. The volume ratio of maternal versus zygotic seed tissues changes considerably among species and underlies different nutrient-storing strategies. Such diversity arose through the evolution of cell elimination programs that regulate the relative growth of one tissue over another to become the major stor- age compartment. The elimination of the nucellus maternal tissue is regulated by developmental programs that marked the origin of angiosperms and outlined the most ancient seed architectures. This review focuses on such a defining mechanism for seed evolution and discusses the role of nucellus development in seed tissues and nutrient partitioning at the light of novel discoveries on its molecular regulation. Keywords Ovule · Seed · Nucellus · Perisperm · Endosperm · Partitioning Introduction fertilization product (Fig. 1) (Linkies et al. 2010). Angio- sperm seeds have been classified into three major architec - Tissue partitioning is the driving force that shapes the tures according to the relative volumes of the fertilization development of different seed structures. The relative con - products, embryo and endosperm, and the nucellus (Fig. 1). tribution of each tissue to the final seed mass varies con - In mature endospermic seeds (e.g., cereals), the endosperm siderably among species and underlies different nutrient- surrounds the embryo and plays an important role in nutri- storing strategies. Tissue partitioning is achieved through ent storing (Sreenivasulu and Wobus 2013). By contrast, the cell elimination programs that regulate the degeneration of endosperm of non-endospermic seeds (e.g., most legumes) one tissue in favor of another (Ingram 2017). The nucel- is completely consumed by the embryo, which becomes the lus, the most distal maternal tissue of the ovule primordium primary storage tissue (Weber et al. 2005). Finally, perisp- (the seed precursor) responsible for the formation of the ermic seeds (e.g., pseudocereals such as amaranth and qui- female gametophyte, plays a key role in defining the seed noa) develop a large perisperm, a tissue originating from the structure together with the fertilization product/s. In gym- nucellus, along with a minute endosperm (Burrieza et al. nosperms, most of the nucellus is eliminated and replaced 2014). The ancestral condition of angiosperm seeds is still by the female gametophyte, the main storage tissue, which debated between endospermic and perispermic as basal will be in turn absorbed by the developing embryo, the only angiosperms display either a large nucellus or endosperm as primary seed storage compartment (Friedman and Bachelier 2013). Plants shifted several times between the endospermic A contribution to the special issue ‘Seed Biology’. and perispermic seed condition highlighting the antagonis- tic development of endosperm and nucellus as a defining Communicated by L. Lepiniec, H. North, G. Ingram. mechanism for seed evolution. Recent discoveries on the molecular regulation of nucellus * Enrico Magnani firstname.lastname@example.org elimination have given an insight into the process of seed tissues partitioning. Here, we discuss them in the context of angiosperm Institut Jean-Pierre Bourgin, INRA, AgroParisTech, CNRS, seed natural diversity. Finally, we review nutrient transport and University of Paris-Saclay, Route de St-Cyr (RD10), accumulation in the nucellus across different seed architectures 78026 Versailles Cedex, France to present seed tissue and nutrient partitioning as two coherent Ecole Doctorale 567 Sciences du Végétal, University and inextricably linked aspects of seed development. Paris-Sud, University of Paris-Saclay, Bat 360, 91405 Orsay Cedex, France Vol.:(0123456789) 1 3 310 Plant Reproduction (2018) 31:309–317 general distinction is made between ovules that bear nucellus hypodermal cells above the megaspore mother cell (MMC) (crassinucellar) and those that display only distal epider- mal nucellus cells (tenuinucellar). Crassinucellar ovules are considered ancestral to tenuinucellar, as they are present in basal angiosperms, magnoliids, most monocots, and basal and part of the core eudicots. They are further classified into (1) truly crassinucellar, if they carry two or more distal hypodermal nucellus cell layers, (2) weakly crassinucellar when they display only one hypodermal cell layer, or (3) pseudo-crassinucellar if the distal nucellus epidermal cell layer divides periclinally to form additional cell layers, in the absence of hypodermal cells. The tenuinucellar condition, observed in several monocots and part of the core eudicots, includes (4) incompletely tenuinucellar ovules, which dis- play hypodermal nucellus cells proximal and/or lateral to the MMC, (5) truly tenuinucellar ovules, without any hypo- dermal nucellus cell, and (6) reduced tenuinucellar ovules, when the proximal region of the MMC is not fully enclosed by the nucellus. Further terminology has been created to describe specific nucellus regions. In pseudo-crassinucellar ovules, the dermal layers of the nucellus apex (at the micro- pylar region) undergoing periclinal cell divisions are called “nucellar cap.” In extreme cases, the nucellus apex divides massively to form a “nucellar beak” that can extend outside the seed coat and define the micropyle. Nucellus epidermal cells can also elongate radially around the female gameto- phyte to form a so-called nucellar pad (Johri et al. 2013). A persistent nucellus base, at the chalazal side, is instead referred to as “podium” or “postament” if only its axial part persists (Johri et al. 2013). Overall, this classification highlights the great natural diversity in ovule nucellus size, which sets the premises for tissue partitioning programs later on in development. Nucellus architecture changes during ovule and seed development. The female gametophyte grows at the expense of the nucellus which is partially eliminated, a process that is still almost completely unexplored (Johri et al. 2013). After fertilization, the nucellus of endospermic and non-endosper- mic seeds partially degenerates to make space to endosperm and embryo growth. By contrast, perispermic seeds display a large central nucellus (perisperm) that grows to become the Fig. 1 Seed architectures. Diagrammatic representation in longitu- main storage tissue along a minute endosperm. Variations dinal sections of pine (gymnosperm) (a), Arabidopsis (angiosperm, have been observed in between these extreme seed architec- endospermic) (b), rice (angiosperm, endospermic) (c), and quinoa (angiosperm, perispermic) (d) seeds right after fertilization and at an tures. A retard in the elimination of the nucellus is a hall- early embryogenesis stage. The figure is not in scale. Female game- mark of coffee grains. In coffee, the nucellus grows to define tophyte, nucellus, endosperm, and embryo are highlighted in violet, seed size and is then replaced by the endosperm (Alves et al. orange, blue, and yellow, respectively 2016; Mayne 1937). Similarly, the nucellus of Austrobai- leya scandens seeds drives early seed growth and is then Natural diversity in nucellus morphology eliminated by the endosperm, whose further development determines final seed size (Losada et al. 2017). By contrast, Angiosperm ovules have been classified according to their nucellus and endosperm coexist and display a similar vol- nucellus position and thickness (Endress 2011). A first ume in Acorus calamus seeds (Floyd and Friedman 2000). 1 3 Plant Reproduction (2018) 31:309–317 311 Furthermore, the structure of Malpighiaceae seeds appears the rest of the ovules to form a gate between chalaza and perispermic during early seed development but the nucel- endosperm till embryo maturity (Xu et al. 2016). lus is fully eliminated by the embryo at later stages (Souto Elimination of the nucellus, as well as seed coat growth, and Oliveira 2014). Finally, Podostemaceae ovules do not is triggered by the endosperm (Fig. 2) (Roszak and Kohler undergo central cell fertilization and lack an endosperm. In 2011; Xu et al. 2016). Single fertilization of the central cell these species, the nucellus cell walls proximal to the female is necessary and sufficient to initiate nucellus degeneration. gametophyte break down to produce a multinucleate cyto- The MADS box transcription factor AGAMOUS LIKE 62 plasmic structure termed “nucellar plasmodium” (Arekal (AGL62) is specifically expressed in the endosperm and and Nagendran 1975, 1977). essential for nucellus–endosperm communication. agl62 A mechanical role for the nucellus has also been hypoth- mutant seeds display precocious endosperm cellulariza- esized. The anticlinal cell walls of the rice nucellus epi- tion and fail to undergo nucellus degeneration and seed coat dermis, surrounding the endosperm, are uniquely thickened differentiation. Figueiredo and co-workers have recently with cellulosic material and have been speculated to pro- proposed that AGL62 regulates auxin efflux, considered vide mechanical support (Krishnan and Dayanandan 2003). the fertilization signal that coordinates the development of Similarly, the chalazal or micropylar nucellus cells can dif- endosperm and maternal tissues (Figueiredo et al. 2016). ferentiate into the so-called hypostase and epistase, respec- Nevertheless, this model has been tested solely on seed coat tively. The cell walls of these nucellar structures thicken growth and not on nucellus degeneration. Two alternative and accumulate cutin, suberin, lignin, or callose. Hypostase scenarios have been proposed to explain nucellus elimina- and epistase have not been assigned a clear function yet but tion: The endosperm might generate mechanical signals are thought to play a mechanical role or work as apoplastic while growing against the nucellus or act as strong nutrient barriers (Johri et al. 2013). sink, thus triggering death of neighboring tissues by nutri- ent deprivation (Ingram 2017). It has been argued that the latter two models are less favorable to explain endosperm- maternal tissue developmental coordination as titan 2 mutant Tissue partitioning seeds, which undergo early endosperm arrest comparable to agl62 (Liu and Meinke 1998), show signs of seed coat Nucellus elimination in Arabidopsis growth (Roszak and Kohler 2011) and nucellus degeneration (personal observations). In Arabidopsis seeds, nucellus elimination begins 2 days Regardless of the nature of the signaling mechanism, it after flowering (DAF) and progresses in a distal–proximal has been shown that endosperm growth relieves the repres- fashion to achieve the loss of 50% of its cells by 8 DAF. A sive action mediated by Fertilization-Independent Seed (FIS) few layers of proximal nucellus cells persist and expand with Polycomb Group (PcG) proteins on nucellus degeneration (Xu et al. 2016). Compared to other FIS genes that are solely Fig. 2 Signaling pathways underlying nucellus and endosperm antagonistic development. Arrows indicate functional relationships 1 3 312 Plant Reproduction (2018) 31:309–317 expressed in the ovule central cell, Fertilization-Independent whose symplastic connection with the chalaza is interrupted Endosperm (FIE) and Multicopy Suppressor of IRA1 (MSI1) (Dwivedi et al. 2014; Maness and McBee 1986; Wang are also expressed in the nucellus and seed coat (Kohler et al. et al. 2012). Rice, Brachypodium, barley, and wheat grains 2003; Xu et al. 2016). Both fie/+ and msi1/+ mutants display develop instead the so-called nucellar projection, a tissue high penetrance of autonomous seed coat growth (Roszak dedicated to nutrient transport simplastically connected to and Kohler 2011) and nucellus degeneration (Xu et al. 2016) the placenta (Krishnan and Dayanandan 2003; Opanowicz in the absence of fertilization. Downstream of PcG proteins, et al. 2011; Oparka and Gates 1981; Radchuk et al. 2009, TRANSPARENT TESTA 16 (TT16) and GORDITA (GOA) 2011; Wang et al. 1994a, b, 1995; Zheng and Wang 2011). MADS BOX transcription factors promote nucellus elimina- The nucellar projection of barley and wheat grains is more tion and inhibit cell division (Xu et al. 2016). TT16 regulates developed and has been divided into different regions based nucellus cell elimination in part by repressing the expres- on cell morphology: (starting from the integument inward) sion of HVA22d, which inhibits gibberellin-mediated pro- (1) actively dividing cells, (2) elongating cells, (3) trans- grammed cell death (PCD) and autophagy. Furthermore, a fer cells with wall ingrowth, and (4) cell debris (Radchuk papain-type KDEL-tailed cysteine endopeptidase (CysEP), et al. 2006; Thiel et al. 2008; Wang et al. 1994a; Zheng and involved in PCD of vegetative tissues, has been shown to Wang 2011). By contrast, the nucellus epidermis of rice and be expressed in the distal nucellus undergoing degenera- Brachypodium appears larger and more persistent, compared tion (Zhou et al. 2016). Nevertheless, nucellus elimination to other cereals (Ellis and Chaffey 1987; Opanowicz et al. has not been entirely assigned to any known cell death pro- 2011; Oparka and Gates 1981). Finally, the chalazal nucellus gram. As in vacuolar PCD (van Doorn et al. 2011), nucellus physically touches the endosperm in maze, Brachypodium, cells undergo autophagy. By contrast, the nucellus displays and rice, while it is separated by a cavity filled with nucel- protoplast shrinkage and largely unprocessed cell corpses, lar lysate (referred to as “endosperm or nucellar cavity” or which are hallmarks of necrosis (van Doorn et al. 2011). “placental sac”) in wheat, barley, and sorghum. Another example of PCD that combines signs of vacuolar The Arabidopsis signaling pathway underlying nucellus and necrotic cell death is induced by the successful recogni- development is partially conserved in rice grains (Fig. 2). tion of pathogens during hypersensitive response (HR) (van The rice TT16 orthologous gene, MADS29, is expressed in Doorn et al. 2011). Nevertheless, PCD associated with HR the nucellus and nucellar projection and promotes cell elimi- does not exhibit degradation of the cell wall as in the nucel- nation (Nayar et al. 2013; Yang et al. 2012; Yin and Xue lus. Furthermore, mutations in the METACASPASE1 and 2012). Compared to Arabidopsis, MADS29 is also expressed LESION SIMULATING DISEASE1 genes, which encode in the embryo and the protein has been detected in nucellus components of the HR-PCD machinery (Coll et al. 2010), epidermis, embryo, and endosperm but not in the nucellar do not affect nucellus development (Xu et al. 2016). projection (Nayar et al. 2013). MADS29 directly activates As endosperm growth is necessary to initiate nucellus the expression of nucleotide-binding site–leucine-rich repeat elimination, the persistence of the nucellus in tt16 mutant proteins and Cys proteases (Yin and Xue 2012). In line with seeds negatively affects endosperm development revealing the Arabidopsis endosperm-maternal tissue signaling model an antagonistic development of endosperm and nucellus (Xu (Figueiredo et al. 2016), MADS29 expression is induced by et al. 2016). This antagonism is reflected in the evolution auxin and regulates auxin–cytokinin homeostasis (Nayar of the two most ancient seed structures, perispermic and et al. 2013; Yin and Xue 2012). Furthermore, antagonistic endospermic, which rely on nucellus or endosperm as major development of nucellus and endosperm has been observed storage tissue, respectively. also in rice as suppression of MADS29 expression impairs starch accumulation and endosperm growth (Nayar et al. Nucellus elimination in cereals 2013; Yang et al. 2012; Yin and Xue 2012). In barley grains, nucellus elimination correlates with the In cereals, the nucellus accounts for most of the grain volume expression of genes encoding for Asp protease-like protein at anthesis and it is eliminated after fertilization in a centrip- nucellin, vacuolar processing enzyme nucellain, Cys and etal fashion. At grain filling, only the outermost nucellus Asp endopeptidases, subtilisin-like Ser proteinases, and cell layer (nucellus epidermis) and a few nucellus cell layers JEKYLL protein, all known to play a role in PCD (Chen overlaying the ovule vascular trace at the chalazal side are and Foolad 1997; Linnestad et al. 1998; Radchuk et al. 2006, retained and undergo PCD more or less rapidly according to 2011, 2018; Thiel et al. 2008; Tran et al. 2014). Down-regu- the species. The chalazal nucellus of maize grains appears lation of jekyll by RNA interference affects nucellus elimina- as compact layers of dead cells with limited plasmodesmata tion and nucellar projection differentiation and, indirectly, connections (Felker and Shannon 1980; Kladnik et al. 2004). endosperm development and starch accumulation (Rad- In sorghum, the chalazal nucellus consists of a few large cell chuk et al. 2006). Furthermore, the differentiation gradient layers which are reduced to one during development and along the barley nucellar projection is also regulated by a 1 3 Plant Reproduction (2018) 31:309–317 313 gibberellin-to-abscisic acid balance, with gibberellin pro- of hydrogen peroxide, nitric oxide, and ethylene, which has moting differentiation (Weier et al. 2014). been proposed as the signaling molecule between endosperm Morphological analyses of nucellus parenchymal cells in and nucellus (Lombardi et al. 2007, 2010, 2012). High level wheat revealed fragmentation of the cytoplasm, vacuoliza- of indole acetic acid has also been detected in endosperm tion, disruption of the nuclear envelope and plasma mem- and nucellus of Sechium edule seeds but its role in nucellus brane, and mitochondrion structural alterations (Dominguez development is still unclear (Lombardi et al. 2012). By con- et al. 2001). Nevertheless, the authors of this study might trast, the nucellus of peach seeds displays a pick of abscisic have erroneously located nucellus cells as what it is indi- acid after anthesis, thus suggesting that different hormones cated as nucellus parenchymal cell in Fig. 2b appears to might play a role in nucellus degeneration in different spe- be integument cells. In line with this interpretation, the cies (Piaggesi et al. 1991). cells analyzed do not undergo degeneration of the cell wall. Nucellus epidermis and nucellar projection of wheat grains Nucellus retention have been shown to express genes encoding for carboxy- peptidase III, thiol protease, nucellain, and nucellin, some Perispermic seeds such as quinoa, amaranth, Peperomia, of which are also implicated in aleurone death during germi- spinach, and Nymphaeales display a large nucellus, which nation (Domınguez and Cejudo 1998; Drea et al. 2005). A defines seed size and becomes the major storage tissue, parallel has been drawn between wheat and Brachypodium along a minute endosperm. The process has been well stud- nucellus, which also expresses nucellain during its elimina- ied in quinoa. At anthesis, the nucellus reaches its final num- tion (Opanowicz et al. 2011). ber of cells as its mitotic activity arrests. After fertilization, Finally, the study of the maize invertase Miniature 1 a relatively small endosperm grows at the expense of part (Mn1) gene revealed a mechanical interaction between of the nucellus and leads the way to embryo development nucellus and endosperm. Maize grains mutated for the Mn1 which in turn consumes most of the endosperm and part of gene show a gap between the nucellus cells, which are rap- the nucellus. The central nucellus, termed perisperm, is not idly emptied of their nuclear and cytoplasmic material, and eliminated and undergoes cell expansion, endoreduplication, the endosperm. Such a gap is not due to cell death but to reserve accumulation, and PCD. Nucellus cell death involves an underdeveloped endosperm that results in over-expanded nuclease and proteolytic activity but not cell wall degen- nucellus cells, thus suggesting that the endosperm exercises eration, a process comparable to endosperm cell death in a mechanical force on the nucellus (Kladnik et al. 2004). endospermic seeds (Burrieza et al. 2014; Lopez-Fernandez Overall, these data indicate that a protease-dependent cell and Maldonado 2013). death machinery is shared by cereals to achieve nucellus degeneration. These same types of proteases, even though not necessarily the same genes, appear to drive endosperm Nutrient partitioning cell death. On the other hand, more data are necessary to highlight variations in the nucellus elimination pathways Tissue and nutrient partitioning are two inextricably linked responsible for the slightly different nucellus fates observed processes. Such a diverse panorama of seed structures cor- in different cereals. relates therefore with an equally broad spectrum of nutri- ent-storing strategies. What all angiosperm seeds have in Nucellus elimination in other angiosperms common is the allocation of resources from the placental maternal tissue, through the chalaza, to the storage tissues Similar to Arabidopsis and cereals, a number of other following a source-sink nutrient gradient (Patrick and Offler angiosperm seeds have been shown to undergo early nucel- 2001). In most angiosperms, vascularization arrests at the lus elimination in a progressive fashion starting from the chalaza, and nutrients follow a combination of symplastic nucellus–endosperm border toward the chalazal region. and apoplastic pathways to reach the sink tissues. Neverthe- Proteomics and genetic analyses revealed the presence of less, there are examples of nucellar tracheids, an ancestral Cys endopeptidases and other peptidases associated with character also observed in extinct gymnosperms, and vas- PCD in the nucellus of castor bean seeds (Greenwood et al. cularized seed coats (Johri et al. 2013). 2005; Nogueira et al. 2012). Cys endopeptidases are accu- mulated in ricinosomes, organelles derived from the endo- Sugar transport in endospermic seeds plasmic reticulum that collapse upon nucellus degeneration releasing their content in the cytoplasm and contributing The role of the nucellus in nutrient transport has been mostly to the digestion of proteinaceous debris (Greenwood et al. addressed studying cereal grain filling. In cereals, nutri- 2005). In Sechium edule, nucellus elimination correlates ents are supposed to travel simplastically from the phloem with the induction of caspase-like proteases and high levels through the maternal tissues of the chalazal region to then 1 3 314 Plant Reproduction (2018) 31:309–317 being released into the apoplast. The endosperm, which is the importance of this tissue in nutrient partitioning (Melkus not simplastically connected to the maternal tissues, uploads et al. 2011; Radchuk et al. 2006; Rolletschek et al. 2011). nutrients from the apoplast and accumulates mostly starch Rice and Brachypodium grains develop a smaller nucel- while undergoing PCD (Thorne 1985). The nucellus lies at lar projection than barley and wheat, but display a thicker the interface of maternal and endosperm tissues and can play nucellus epidermis which has been proposed to play an a role in nutrient transfer. active role in nutrient transport (Ellis and Chaffey 1987; In maize grains, sucrose moves simplastically from the Opanowicz et al. 2011; Oparka and Gates 1981). Defective phloem to the chalaza and is then released into the apoplast starch synthesis in the endosperm has been observed in rice where cell wall-bound invertases convert it into hexoses, grains with suppressed MADS29 expression, highlighting glucose and fructose (Felker and Shannon 1980; McLaugh- the active role of the rice nucellus in transferring nutrients lin and Boyer 2004; Porter et al. 1985; Shannon 1972a, b; to the endosperm (Nayar et al. 2013; Yin and Xue 2012). Tang and Boyer 2013). The nucellus is not simplastically During nutrient transfer, the nucellus might act as a short- connected to the chalaza and imports glucose during the term sink as MADS29 has been found to promote the dif- first stages of grain development while being eliminated ferentiation of proplastids in amyloplasts likely by regulating by endosperm growth (McLaughlin and Boyer 2004; Tang cytokinin biosynthesis (Nayar et al. 2013). Finally, SWEET and Boyer 2013). Later in development, persistent nucel- sucrose exporters have been found in all rice nucellar tissues, lus cells undergo PCD (Felker and Shannon 1980; Kladnik indicating that the nucellus engages in apoplastic seed filling et al. 2004), thus suggesting that nutrients cross the nucellus (Yang et al. 2018). apoplastically. A similar path of sugar transport probably occurs in sorghum grains as they accumulate hexoses in the Sugar transport in perispermic seeds placental sac and display symplastic disconnection of cha- laza and nucellus (Dwivedi et al. 2014; Maness and McBee The role of the nucellus in perispermic seeds changes from 1986; Wang et al. 2012). nutrient-transport facilitator to long-term nutrient sink. By contrast, the nucellus of wheat and barley is simplasti- The perisperm of quinoa seeds accumulates mostly starch cally connected to the placenta and the nucellar projection while undergoing PCD (Lopez-Fernandez and Maldonado develops transfer cells, thus expanding the nutrient unload- 2013). Starch accumulation follows an apical–basal pat- ing zone and facilitating transfer (Radchuk et al. 2009, tern, with the chalazal side being the last to be filled. Such 2011; Wang et al. 1994a, b, 1995; Zheng and Wang 2011). a pattern might be the result of sugars transport from the At the beginning of barley seed development, starch accu- chalaza toward the perisperm while maximizing seed filling mulates mostly in the pericarp, which acts as a short-term by following a source-sink gradient. Alternatively, nutrient sink, and only transiently in the nucellus. Alpha amylase transport through the seed coat might also explain such a 4 is expressed in degenerating nucellus tissue facilitating nutrient accumulation pattern. At seed maturity, perisperm mobilization of starch toward the endosperm during nucel- cells appear as thin walled and completely filled with starch lus elimination (Radchuk et al. 2006, 2009). At barley grain grains, similar to cereal starchy endosperm cells (Lopez- filling, C sucrose analyses revealed a flow of sucrose from Fernandez and Maldonado 2013; Prego et al. 1998). By con- the nucellar projection toward the endosperm (Melkus et al. trast, the role of the few endosperm cells that persist at the 2011; Rolletschek et al. 2011). The nucellus projection of micropylar region is less clear. barley grains expresses a cell wall-bound invertase, indicat- ing that hexoses are also released into the endosperm cavity (Weschke et al. 2003). Furthermore, barley nucellar projec- tion and epidermis express members of the aquaporin family, Conclusive remarks which may play a role in nutrient efflux (Thiel et al. 2008). Interestingly, transfer cells of the nucellar projection and The evolution of seed storage tissues in angiosperms has endosperm of barley and wheat express the same sucrose been a “battle” between endosperm and nucellus develop- symporter (SUT) genes responsible for sucrose import in ment. Both tissues can store starch and become the main sink tissues (Bagnall et al. 2000; Weschke et al. 2000). source of energy for embryo germination. Indeed, the The role of SUT proteins in the nucellus is not clear, and nucellus of perispermic seeds parallels the endosperm of it might allow sucrose scavenging, work as sucrose passive endospermic seeds at both morphological and functional lev- port along concentration gradient or be an evolutionary relic els. Nevertheless, most angiosperm seeds evolved mutually of perispermic seeds. Impaired development of the barley exclusive growth of nucellus and endosperm. The nucellus nucellar projection leads to starch accumulation in maternal offers an easier system of nutrient storage simplastically con- tissues at the expense of the endosperm, thus further proving nected to the placenta. By contrast, the endosperm couples 1 3 Plant Reproduction (2018) 31:309–317 315 caryopsis development. Plant Cell 17:2172–2185. h t t p s : / / d o i . nutrient storing to fertilization, thus possibly avoiding org/10.1105/tpc.105.03405 8 energy waste in case of unsuccessful fertilization. Dwivedi KK, Roche DJ, Clemente TE, Ge Z, Carman JG (2014) The Whereas we have a better understanding on seed nutrient OCL3 promoter from Sorghum bicolor directs gene expression to transport and tissue elimination, the next challenge will be to abscission and nutrient-transfer zones at the bases of floral organs. Ann Bot 114:489–498. https ://doi.org/10.1093/aob/mcu14 8 address how nutrient and tissue partitioning are coordinated Ellis JR, Chaffey NJ (1987) Structural differentiation of the nucel- at the molecular level. lar epidermis in the caryopsis of rice (Oryza sativa). Ann Bot 60:671–675 Author contribution statement JL reviewed the role of Endress PK (2011) Evolutionary diversification of the flowers in angiosperms. Am J Bot 98:370–396. https ://doi.org/10.3732/ MADS box genes in nucellus development. EM wrote the ajb.10002 99 rest of the paper in consultation with JL. Felker FC, Shannon JC (1980) Movement of C-labeled assimilates into kernels of Zea mays L.: III. An anatomical examination and microautoradiographic study of assimilate transfer. Plant Funding This work was supported by the INRA BAP starter, Labex Physiol 65:864–870 Saclay Plant Sciences-SPS (ANR-10-LABX-0040-SPS), and China Figueiredo DD, Batista RA, Roszak PJ, Hennig L, Kohler C (2016) Scholarship Council Ph.D. grants. Auxin production in the endosperm drives seed coat develop- ment in Arabidopsis. Elife. https ://doi.org/10.7554/elife .20542 Floyd SK, Friedman WE (2000) Evolution of endosperm develop- Open Access This article is distributed under the terms of the Crea- mental patterns among basal flowering plants. 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