Live and Let Die - The Bsister MADS-Box Gene OsMADS29 Controls the Degeneration of Cells in Maternal Tissues during Seed Development of Rice (Oryza sativa)

Abstract

Bsister genes have been identified as the closest relatives of class B floral homeotic genes. Previous studies have shown that Bsister genes from eudicots are involved in cell differentiation during ovule and seed development. However, the complete function of Bsister genes in eudicots is masked by redundancy with other genes and little is known about the function of Bsister genes in monocots, and about the evolution of Bsister gene functions. Here we characterize OsMADS29, one of three MADS-box Bsister genes in rice. Our analyses show that OsMADS29 is expressed in female reproductive organs including the ovule, ovule vasculature, and the whole seed except for the outer layer cells of the pericarp. Knock-down of OsMADS29 by double-stranded RNA-mediated interference (RNAi) results in shriveled and/or aborted seeds. Histological analyses of the abnormal seeds at 7 days after pollination (DAP) indicate that the symplastic continuity, including the ovular vascular trace and the nucellar projection, which is the nutrient source for the filial tissue at early development stages, is affected. Moreover, degeneration of all the maternal tissues in the transgenic seeds, including the pericarp, ovular vascular trace, integuments, nucellar epidermis and nucellar projection, is blocked as compared to control plants. Our results suggest that OsMADS29 has important functions in seed development of rice by regulating cell degeneration of maternal tissues. Our findings provide important insights into the ancestral function of Bsister genes.

Endosperm and Nucellus Develop Antagonistically in Arabidopsis Seeds

“…The integuments undergo a rapid phase of cell division and expansion and follow different cell fates (Haughn and Chaudhury, 2005). In several plant species, the proximal region of the nucellus undergoes programmed cell death (PCD) and partially or totally disappears (Domínguez et al, 2001;Hiratsuka et al, 2002;Krishnan and Dayanandan, 2003;Greenwood et al, 2005;Lombardi et al, 2007;Radchuk et al, 2011;Yang et al, 2012;Yin and Xue, 2012). By contrast, the perisperm of quinoa seeds accumulates starch and follows a slower cell death program that retains the cell wall (López-Fernández and Maldonado, 2013).…”

“…By contrast, the perisperm of quinoa seeds accumulates starch and follows a slower cell death program that retains the cell wall (López-Fernández and Maldonado, 2013). In some cereal grains, the nucellus cells positioned between the vascular bundle and the endosperm, termed the nucellar projection, undergo PCD but persist during seed development and become transfer cells (Domínguez et al, 2001;Yang et al, 2012;Yin and Xue, 2012). Proteases, nucleases, vacuolar processing enzymes, and JEKYLL proteins have all been implicated in nucellus PCD (Chen and Foolad, 1997;Dominguez and Cejudo, 1998;Linnestad et al, 1998;Radchuk et al, 2006Radchuk et al, , 2011Sreenivasulu et al, 2006;Lombardi et al, 2007;Nogueira et al, 2012;Yin and Xue, 2012;López-Fernández and Maldonado, 2013).…”

“…The regulation of nucellus development has been partially elucidated in rice (Oryza sativa), an endospermic species. The rice MADS box transcription factor MADS29 promotes nucellus PCD by regulating the expression of cysteine proteases and nucleotide binding site-Leu-rich repeat proteins (Yang et al, 2012;Yin and Xue, 2012).…”

Heat stress yields a unique MADS box transcription factor in determining seed size and thermal sensitivity

“…Misregulation of one of the potential rice homologs of PHE1, OsMADS87, correlated with an altered developmental transition in interspecies rice crosses (Ishikawa et al, 2011). Besides type I MADS box genes, other subgroup members such as OsMADS29 also play a critical role in normal rice seed development (Yang et al, 2012;Yin and Xue, 2012;Nayar et al, 2013).…”

OsMADS26 negatively regulates resistance to pathogens and drought tolerance in rice.

“…Most of the studied genes are involved in the control of development, including tillering, flower development, and flowering time (Arora et al, 2007;Guo et al, 2013). Some of them are involved in development by controlling stress-related processes, such as OsMADS3, which is involved in reactive oxygen species homeostasis during anther development, and OsMADS29, which controls cell degeneration during seed development (Hu et al, 2011;Yang et al, 2012). A possible specific involvement of rice MADS genes in stress response has been reported only for OsMADS26, the rice ortholog of AGL12 (Lee et al, 2008b.…”