miR156-Targeted and Nontargeted SBP-Box Transcription Factors Act in Concert to Secure Male Fertility in Arabidopsis    

Abstract

The SBP-box transcription factor SQUAMOSA PROMOTER BINDING PROTEIN-LIKE8 (SPL8) is required for proper development of sporogenic tissues in Arabidopsis thaliana. Here, we show that the semisterile phenotype of SPL8 lossof-function mutants is due to partial functional redundancy with several other members of the Arabidopsis SPL gene family. In contrast with SPL8, the transcripts of these latter SPL genes are all targeted by miR156/7. Whereas the introduction of single miR156/7-resistant SPL transgenes could only partially restore spl8 mutant fertility, constitutive overexpression of miR156 in an spl8 mutant background resulted in fully sterile plants. Histological analysis of the anthers of such sterile plants revealed an almost complete absence of sporogenous and anther wall tissue differentiation, a phenotype similar to that reported for sporocyteless/nozzle (spl/nzz) mutant anthers. Expression studies indicated a functional requirement for miR156/7-targeted SPL genes limited to early anther development. Accordingly, several miR156/7-encoding loci were found expressed in anther tissues at later stages of development. We conclude that fully fertile Arabidopsis flowers require the action of multiple miR156/7-targeted SPL genes in concert with SPL8. Either together with SPL/NZZ or independently, these SPL genes act to regulate genes mediating cell division, differentiation, and specification early in anther development. Furthermore, SPL8 in particular may be required to secure fertility of the very first flowers when floral transition-related miR156/7 levels might not have sufficiently declined.

The control of developmental phase transitions in plants

“…dependent on the position of the flower in the inflorescence and not only to environmental variation (Diggle, 2002). Interestingly, miR156-targeted SPL genes function redundantly with the SPL8 gene, which is not targeted by miR156, in promoting Arabidopsis flower fertility (Xing et al, 2010). Furthermore, miR156-targeted SPL gene activity has recently been coupled to increasing flavonol to anthocyanin ratios within the developing Arabidopsis shoot (Gou et al, 2011).…”

“…In Arabidopsis, the targets of miR156 include transcripts of 11 of the 17 SPL genes, and other miR156 targets that represent orthologues or likely orthologues of SPL-like genes have been identified in other species (summarized in Table 1). Experimental evidence that the miRNA recognition elements (MREs) of these transcripts are indeed responsive and functional is diverse and convincing (Franco-Zorrilla et al, 2007;Martin et al, 2010b;Park et al, 2005;Schwab et al, 2005;Shikata et al, 2009;Usami et al, 2009;Wang et al, 2009;Wang et al, 2008;Wu et al, 2009;Wu and Poethig, 2006;Xing et al, 2010).…”

Transcriptional control of flavonoid biosynthesis

“…20,21 These plantspecific SPB-box proteins are known to influence a large array of developmental processes in Arabidopsis, such as promoting the juvenile-to-adult phase transition by activating miR172, inducing flowering via activating LEAFY and the MADS box genes, inhibiting trichome initiation on floral organs through activating TCL1, as well as concertedly controlling male fertility. [21][22][23][24] Recently, the miR156/157-targeted SPLs have been shown to affect metabolic fluxes through the branched flavonoid biosynthetic pathway. 4 Dihydroflavonols serve as common precursors of flavonols and anthocyanins and can be oxidized either by FLS to form flavonols or reduced by DFR to produce leucoanthocyanidins in the first dedicated step for anthocyanin biosynthesis (Fig.…”

ThemicroRNA156-SQUAMOSA PROMOTER BINDING PROTEIN-LIKE3Module Regulates Ambient Temperature-Responsive Flowering viaFLOWERING LOCUS Tin Arabidopsis

“…Examples of such modules in the Arabidopsis (Arabidopsis thaliana) and other plant species include microRNA156 (miR156) and its targets, namely SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) genes. These miR156-SPL regulatory modules are known to play a central role in the regulation of diverse developmental processes (Schwarz et al, 2008;Wang et al, 2008;Nodine and Bartel, 2010;Xing et al, 2010;Yu et al, 2010;Gou et al, 2011;Yang et al, 2011). The miR156-SPL3 module has been identified as part of a regulatory mechanism that can induce flowering in the absence of photoperiodic cues ).…”