Functionally redundant SHI family genes regulate Arabidopsis gynoecium development in a dose‐dependent manner

Abstract

SummaryGene duplication events, and the subsequent functional divergence of duplicates, are believed to be important evolutionary agents, driving morphological diversification. We have studied the structural and functional diversification of members of a plant-specific gene family in Arabidopsis thaliana by analysing mutant phenotypes, expression patterns and phylogeny. The SHI gene family comprises ten members that encode proteins with a RING finger-like zinc finger motif. We show that, despite being highly divergent in sequence, except in two conserved regions, many of the SHI-related genes are partially redundant in function and synergistically promote gynoecium, stamen and leaf development in Arabidopsis. Gynoecia of the loss-offunction sty1-1 mutant display subtle morphological defects, and, although mutations in the related STY2, SHI, SRS3, SRS4, SRS5, SRS7 and LRP1 genes have no apparent effect on gynoecium development, the sty1-1 mutant phenotype is gradually enhanced in double, triple, quadruple and quintuple mutant combinations, suggesting a remarkably extensive functional conservation within the family, which appears to be based on dosage dependency and protection against dominant negative mutations. In multiple mutant lines, all marginal tissues in the apical part of the gynoecium are dramatically reduced or missing, and our data indicate that SHI family members may promote formation of these tissues downstream of the transcriptional corepressor LEUNIG (LUG).

Expression of ArabidopsisSHORT INTERNODES/STYLISHFamily Genes in Auxin Biosynthesis Zones of Aerial Organs Is Dependent on a GCC Box-Like Regulatory Element

“…SRS4 pro ..GUS is expressed in cotyledon tips, leaf primordia, hydathodes, stipules, and lateral root primordia and weakly at the edges of petals and sepals, demonstrating that its activity largely overlaps with that of the SHI/STY genes studied previously. Kuusk et al (2006) showed that mutations in SRS4 enhanced the leaf phenotype of sty1-1 sty2-1 and, to a limited extent, that of gynoecia, confirming that SRS4 is active in leaves and buds. Additionally, transcriptome analysis (Hruz et al, 2008) reveals low levels of SRS4 transcripts in floral organs.…”

“…The spatial and temporal activities of STY1, STY2, SHI, and SRS5 during plant development have been studied in detail (Fridborg et al, 2001;Kuusk et al, 2002Kuusk et al, , 2006 and were found to be largely overlapping, with some minor exceptions. Using an enhancer/promoter trap approach, Smith and Fedoroff (1995) suggested that LRP1 expression is restricted to lateral root primordia, whereas phenotypic characterizations of multiple SHI/STY mutants carrying a mutation also in LRP1, together with real-time (RT)-PCR data, revealed that LRP1 is expressed at similar sites as STY1, STY2, SHI, and SRS5 also in Arabidopsis aerial tissues .…”

“…2G). The expression of other SHI/ STY family members coincides with that of STY1 in cotyledon tips, leaf primordia, lateral root primordia, receptacles, styles/stigmas, and hydathodes (Fridborg et al, 2001;Kuusk et al, 2002Kuusk et al, , 2006.…”

“…In this line, GUS signal was detected only in lateral root primordia, and the corresponding gene, LRP1, was suggested to be a lateral root primordium-specific gene (Smith and Fedoroff, 1995). However, Kuusk et al (2006) showed that the putative null mutant lrp1 enhances the gynoecium phenotype of the sty1-1 mutant and also that LRP1 transcripts are found by PCR-based methods in floral buds. Our results, implicating the strong lateral root primordium expression of STY1 to be GCC box-independent, explain the spatially limited GUS expression of the lrp1 mutant by suggesting that the GCC box in the 5# UTR of LRP1 does not contribute to activating GUS expression in lrp1.…”

“…This suggests that the phenotypes caused by ectopic 35S promoter-driven DRNL expression might largely be mediated by DRNLinduced ectopic activity of SHI/STY family members. Therefore, we introduced the 35S pro :DRNL-ER construct into a SHI/STY multiple mutant background by crossing the 35S pro :DRNL-ER line with the SHI/STY quintuple mutant (sty1-1 sty2-1 shi-3 lrp1 srs5-1; Kuusk et al, 2006). Progeny of plants homozygous for 35S pro : DRNL-ER and with the severe SHI/STY family multiple mutant phenotype were EST or mock treated.…”