A change in the cell wall status initiates the elimination of the nucellus in Arabidopsis

Abstract

The evolution of the seed habit coincides with 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 in the environment. As a consequence, the nucellus was partially eliminated to accommodate the growth of the female gametophyte inside the sporophyte. With the evolution of angiosperm seeds, the process of nucellus elimination was requisitioned to allow the growth of the endosperm, the second fertilization product devoted to store nutrients. Cell elimination differs from most known cell death programs as it leads to the apparent dismantling of the cell wall. Here, we show that nucellus elimination in Arabidopsis is initiated by the lysis of the pectic polysaccharides in the cell wall. This process exposes other cell wall components to possible further degradation and precedes a cell death program that leads to nuclear DNA fragmentation. Both pathways are regulated by TRANSPARENT TESTA 16, a MADS-domain transcription factor that evolved with seed plants. Finally, the causal effect of cell wall modification on nucellus development is demonstrated by inhibiting pectin degradation, thus suggesting that a change in the cell wall status might have driven seed evolution.