Functional conservation and diversification of class E floral homeotic genes in rice (Oryza sativa)

Abstract

SUMMARYMutant analyses in different eudicotyledonous flowering plants demonstrated that SEPALLATA-like MADSbox genes are required for the specification of sepals, petals, stamens and carpels, and for floral determinacy, thus defining class E floral organ identity genes. SEP-like genes encode MADS-domain transcription factors and constitute an angiosperm-specific gene clade whose members show remarkably different degrees of redundancy and sub-functionalization within eudicots. To better understand the evolutionary dynamics of SEP-like genes throughout the angiosperms we have knocked down SEP-like genes of rice (Oryza sativa), a distant relative of eudicots within the flowering plants. Plants affected in both OsMADS7 and OsMADS8 show severe phenotypes including late flowering, homeotic changes of lodicules, stamens and carpels into palea/ lemma-like organs, and a loss of floral determinacy. Simultaneous knockdown of the four rice SEP-like genes OsMADS1, OsMADS5, OsMADS7 and OsMADS8, leads to homeotic transformation of all floral organs except the lemma into leaf-like organs. This mimics the phenotype observed with the sep1 sep2 sep3 sep4 quadruple mutant of Arabidopsis. Detailed analyses of the spatial and temporal mRNA expression and protein interaction patterns corresponding to the different rice SEP-like genes show strong similarities, but also gene-specific differences. These findings reveal conservation of SEP-like genes in specifying floral determinacy and organ identities since the separation of eudicots and monocots about 150 million years ago. However, they indicate also monocot-specific neo-and sub-functionalization events and hence underscore the evolutionary dynamics of SEP-like genes. Moreover, our findings corroborate the view that the lodicules of grasses are homologous to eudicot petals.

RiceLHS1/OsMADS1Controls Floret Meristem Specification by Coordinated Regulation of Transcription Factors and Hormone Signaling Pathways

“…The latter represent vestiges of lower florets found in other grass spikelets (Bommert et al, 2005). Of the five SEPlike rice genes, OsMADS7 and OsMADS8 are members of SEP3 clade and have retained conserved functions, as they regulate organ development in inner floret whorls (Cui et al, 2010). But members of a grassspecific subgroup in the LOFSEP clade, OsMADS1, OsMADS5, and OsMADS34, have acquired novel functions (Malcomber and Kellogg, 2005;Gao et al, 2010;Kobayashi et al, 2010).…”

“…Mutants in these factors share the phenotype of abnormal extra carpels ( Fig. 2D; Yamaguchi et al, 2006;Dreni et al, 2007;Ohmori et al, 2009;Cui et al, 2010). Protein interactions of OsMADS1 with OsMADS13 (a class D gene), OsMADS7, and OsMADS8 (Favaro et al, 2002;Cui et al, 2010) and its genetic interactions with OsMADS6, OsMADS3, OsMADS58, and OsMADS13 (Dreni et al, 2011;Li et al, 2011aLi et al, , 2011bSupplemental Fig.…”

“…They contribute to panicle morphology, spikelet and FM specification, floral organ differentiation, and meristem determinacy (Jeon et al, 2000;Prasad et al, 2005;Cui et al, 2010;Gao et al, 2010;Kobayashi et al, 2010). Rice LEAFY HULL STERILE (LHS1)/OsMADS1, a member of the grass subgroup of LOFSEP genes, referred to henceforth as OsMADS1, is expressed in FMs, functions during FM establishment and floret organ patterning, and contributes to meristem termination (Jeon et al, 2000;Prasad et al, 2001Prasad et al, , 2005Agrawal et al, 2005;Ohmori et al, 2009;Cui et al, 2010;Gao et al, 2010;Li et al, 2010;Wang et al, 2010). In addition to studies on mutants in rice SEP factors, their protein-protein interactions are reported from yeast two-hybrid analyses.…”

RNase ZS1 processes UbL40 mRNAs and controls thermosensitive genic male sterility in rice

“…Fresh ZH11 young panicles from different developmental stages were fixed immediately, embedded in paraffin (Sigma-Aldrich, USA) and sectioned to 8-mm thickness. Hybridization and immunological detection were performed according to the previously described method 51 . Briefly, sections were over night incubated at 45°C with coverslips in hybridization buffer (40 ml per slide) containing the probes.…”

Jasmonic acid regulates spikelet development in rice

“…To uncover downstream components in the pathway by which JA regulates spikelet development in rice, we analysed the expression of possible target genes in the eg1-3 and eg2-1D mutants. In rice, five E-class (SEPALLATA, SEP) genes (OsMADS1, OsMADS5, OsMADS7, OsMADS8 and OsMADS34) play a key role in specifying inflorescence and spikelet development [38][39][40] . The osmads1 mutant and OsMADS1/5/7/8-RNAi lines display spikelet defect similar to eg1-3 eg2-1D double mutant and some osjaz1-1D gain-of-function lines (Figs 1a and 4f) 15,38 .…”