Conservation of the E-function for Floral Organ Identity in Rice Revealed by the Analysis of Tissue Culture-induced Loss-of-Function Mutants of the OsMADS1 Gene

Abstract

Rapid progress in studies on flower development has resulted in refining the classical 'ABC model' into a new 'ABCDE model' to explain properly the regulation of floral organ identity. Conservation of E-function for flower organ identity among the dicotyledonous (dicot) plants has been revealed. However, its conservation in monocotyledonous (monocot) plants remains largely unknown. Here, we show the conservation of E-function in rice (Oryza sativaL.) by characterizing tissue culture-induced mutants of two MADS-box genes, OsMADS1and OsMADS5, which form a subclade within the well-supported clade of SEP-genes (E-function) phylogeny. Severe loss-of-function mutations of OsMADS1cause complete homeotic conversion of organs (lodicules, stamens, and carpels) of three inner whorls into lemma- and palea-like structures. Such basic deformed structure is reiterated along with the pedicel at the center of the same floret, indicating the loss of determinacy of the flower meristem. These phenotypes resemble the phenotypes caused by mutations of the dicot E-class genes, such as the Arabidopsis SEP123(SEPALLATA1/2/3) and the petunia FBP2(Floral Binding Protein 2), suggesting that OsMADS1play a very similar role in rice to that of defined E-class genes in dicot plants. In case of the loss-of-function mutation of OsMADS5, no defect in either panicles or vegetative organs was observed. These results demonstrate that OsMADS1clearly possesses E-function, and so, E-function is fundamentally conserved between dicot plants and rice, a monocot model plant.

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

“…Under noninductive conditions, when OsMADS1-DGR is sequestered in the cytoplasm, we observe that florets recapitulate strong loss-offunction OsMADS1 mutant phenotypes (Fig. 2, B-E; Jeon et al, 2000;Agrawal et al, 2005;Prasad et al, 2005). The outer floret organs, lemma and palea, were narrow, poorly developed, and failed to enclose the inner organs (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.…”

The AGL6-like gene OsMADS6 regulates floral organ and meristem identities in rice

“…In rice, the B class gene SPW1 (OsMADS16) [20] and the C class genes OsMADS3 and OsMADS58 [21], as well as the D class gene OsMADS13 play critical roles in specifying inner floral organ and meristem identities. OsMADS1/LHS1 has been shown to be a SEP-like gene that is required for determining identity of the lemma/ palea and the meristem of inner floral organs [25][26][27][28][29]. It is possible that OsMADS6 interacts with other MADSbox protein(s) controlling rice flower development.…”

“…Obviously OsMADS6 plays a distinct role in specifying floral organ development from OsMADS1 in rice. Mutations or knockdown of OsMADS1 in rice result in elongated leafy lemma/palea, glume-like organs, a decreased number of stamens, and occasionally, extra pistils or florets [25][26][27][28][29], while mutations of OsMADS6 cause the homeotic transformation of paleas to lemma-like organs, lodicules and stamens into glume-like or mosaic structures. OsMADS6 and Os-MADS1 are both expressed in young floral meristems.…”

“…Rice has diverse SEP-like genes, with at least five members in the genome [24]. Currently, OsMADS1 (also called LEAFY HULL STERILE1, LHS1) is one of the best-characterized SEP-like genes in rice, which has been shown to be required for determining the identity of the lemma/palea and the meristem of inner floral organs [25][26][27][28][29].…”