Endosperm development is an autonomously programmed process independent of embryogenesis

Abstract

The seeds of flowering plants contain three genetically distinct structures: the embryo, endosperm, and seed coat. The embryo and endosperm need to interact and exchange signals to ensure coordinated growth. Accumulating evidence has confirmed that embryo growth is supported by the nourishing endosperm and regulated by signals originating from the endosperm. Available data also support that endosperm development requires communication with the embryo. Here, using single-fertilization mutants, Arabidopsis thaliana dmp8 dmp9 and gex2, we demonstrate that in the absence of a zygote and embryo, endosperm initiation, syncytium formation, free nuclear cellularization, and endosperm degeneration occur as in the wild type in terms of the cytological process and time course. Although rapid embryo expansion accelerates endosperm breakdown, our findings strongly suggest that endosperm development is an autonomously organized process, independent of egg cell fertilization and embryo–endosperm communication. This work confirms both the altruistic and self-directed nature of the endosperm during coordinated embryo-endosperm development. Our findings provide insights into the intricate interaction between the two fertilization products and will help to distinguish the physiological roles of the signaling between endosperm and embryo. These findings also open new avenues in agro-biotechnology for crop improvement.

Endosperm–Embryo Communications: Recent Advances and Perspectives

“…In Arabidopsis, lack of GAMETE-EXPRESSED 2 (GEX2) or DOMAIN OF UNKNOWN FUNC-TION 679 membrane protein 8/9 (DMP8/9) causes singular fertilization with the central cell and leaves the egg cell unfertilized [9][10][11] (Figure 1B). In these mutants, endosperm initiation, syncytium formation, cellularization and degeneration could proceed in the absence of a zygote (embryo) during seed development [1]. Compared to the double-fertilization event, the single fertilization with the central cell only shows slow endosperm breakdown at the final developmental stage (Figure 1A,B).…”

“…Although possessing the same genetic information, the triploid endosperm and the diploid embryo develop towards distinct destinations. In Arabidopsis thaliana, endosperm development undergoes syncytium formation, free nuclei cellularization, and degeneration stages [1][2][3]. In parallel, the zygote gives rise to the mature embryo through morphogenesis and maturation processes [4,5].…”

“…The micropylar and peripheral endosperm nuclei subsequently undergoes cellularization after eight rounds of mitoses, which in Arabidopsis takes place 4 days after pollination (DAP) [7,8]. Soon after cellularization at 5 DAP, the endosperm enters a phase of programmed cell death (PCD) that completes by 9 DAP [1]. During seed development, embryo development relies on endosperm development [3].…”

“…Recent studies using single-fertilization mutants highlighted the independence and autonomous nature of endosperm development from the events of embryogenesis [1]. In Arabidopsis, lack of GAMETE-EXPRESSED 2 (GEX2) or DOMAIN OF UNKNOWN FUNC-TION 679 membrane protein 8/9 (DMP8/9) causes singular fertilization with the central cell and leaves the egg cell unfertilized [9][10][11] (Figure 1B).…”

“…Interestingly, the single-fertilization event that occurrs in the cdka;1 mutant is different from that of the gex2 or the dmp8/9 mutant plants; the former preferably fertilizes egg cell and the latter only fertilizes the central cell. Both types of mutant exhibit fertility defects in the male, not the female [1,12], and it is not clear why they tend to have a preference of which cell to fertilize, the egg cell or the central cell. Although the central cell is not fertilized in the cdka;1 plants, endosperm development does initiate after egg cell fertilization.…”