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.
SBP-box genes represent transcription factors ubiquitously found in the plant kingdom and recognized as important regulators of many different aspects of plant development. In this study, 15 SBP-box gene family members were identified in tomato and analyzed with respect to their genomic organization and other structural features. Phylogenetic reconstruction based on the DNA-binding SBP-domain, allowed the classification of the SlySBP proteins into eight groups representing clear orthologous relationships to family members of other flowering plants and the moss Physcomitrella. In order to have a better understanding of their possible function in the development of a fleshy-fruit species like tomato, the mRNA expression levels of all SlySBP genes were quantified in vegetative and reproductive organs of plants, at different stages of growth. As transcripts of ten SlySBP genes were found to carry putative miR156- and miR157-response elements, the expression levels of the corresponding microRNAs were determined as well, revealing different patterns of expression. In addition, eight putative miR156 and four miR157 encoding loci could be identified in the tomato genome, four of them forming a polycistronic cluster. Whereas miR156 and miR157 levels were highest in seedlings, leaves and anthers of young flowers, most miR156-targeted SlySBP genes were found to be expressed in young inflorescences and during fruit development and ripening, suggesting a particularly important role during tomato reproductive growth. The data presented provide a basis for future clarification of the various functions that SBP-box gene family members play in tomato growth and development.
SPL8 and miR156-targeted SPL genes are known to play an essential role in Arabidopsis anther development. Here we show that these SPL genes are also expressed within the developing gynoecium, where they redundantly control development of the female reproductive tract. Whereas the gynoecium morphology in the spl8 single mutant is largely normal, additional down-regulation of miR156-targeted SPL genes results in a shortened style and an apically swollen ovary narrowing onto an elongated gynophore. In particular, the septum does not form properly and lacks a transmitting tract. Loss of SPL8 function enhances the mutant phenotypes of ett, crc and spt, indicating a functional overlap between SPL8 and these genes in regulating gynoecium development. Furthermore, gynoecium development of 35S:MIR156b spl8-1 double mutants shows enhanced sensitivity to a polar auxin transport inhibitor, and the expression pattern of the auxin biosynthesis gene YUCCA4 is altered compared to wild-type. Our observations imply that SPL8 and miR156-targeted SPL genes control gynoecium patterning through interference with auxin homeostasis and signalling.
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