Seed evolution, a maternal story

Abstract

The evolution of the seed habit can be traced back to a change in the cell fate of the nucellus, the sporophytic tissue responsible for female meiosis. Seeds arose when the nucellus retained the female spores instead of releasing them into the environment. As a consequence, the nucellus was partially eliminated to accommodate the growth of the gametophyte inside the sporophyte. With the evolution of angiosperms, the process of nucellus elimination was co-opted to allow the growth of the endosperm, the second fertilization product devoted to storing nutrients in endospermic seeds such as Arabidopsis and cereals. Alternatively, the nucellus became the main storage tissue of perispermic seeds, such as amaranth and quinoa. Despite the striking differences in nucellus development between endospermic and perispermic seeds, we identified a conserved molecular module responsible for cell elimination, suggesting its ancestral origin. We showed that de-methylesterification and subsequent lysis of the pectic polysaccharides in the cell wall triggers nucellus elimination. This process exposes additional cell wall components to further degradation and initiates nuclear DNA fragmentation. This pathway is regulated by TRANSPARENT TESTA 16, a MADS-domain transcription factor that emerged with seed plants and likely contributed to the ancestral shift in nucellus cell fate. Our results highlight the crucial contribution of extracellular polysaccharides to the development of multicellular organisms.

References

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Lu J., Le Hir R., Gómez-Páez D.M., Coen O., Péchoux C., Jasinski S., Magnani E. The nucellus: between cell elimination and sugar transport. Plant Physiol. 2021 Mar 15;185(2):478-490.