The plant-specific family of WUSCHEL (WUS)-related homeobox (WOX) transcription factors is key regulators of embryogenesis, meristem maintenance, and lateral organ development in flowering plants. The modern/WUS clade transcriptional repressor STENOFOLIA/LAMINA1(LAM1), and the intermediate/WOX9 clade transcriptional activator MtWOX9/NsWOX9 antagonistically regulate leaf blade expansion, but the molecular mechanism is unknown. Using transcriptome profiling and biochemical methods, we determined that NsCKX3 is the common target of LAM1 and NsWOX9 in Nicotiana sylvestris. LAM1 and NsWOX9 directly recognize and bind to the same cis-elements in the NsCKX3 promoter to repress and activate its expression, respectively, thus controlling the levels of active cytokinins in vivo. Disruption of NsCKX3 in the lam1 background yielded a phenotype similar to the knockdown of NsWOX9 in lam1, while overexpressing NsCKX3 resulted in narrower and shorter lam1 leaf blades reminiscent of NsWOX9 overexpression in the lam1 mutant. Moreover, we established that LAM1 physically interacts with NsWOX9, and this interaction is required to regulate NsCKX3 transcription. Taken together, our results indicate that repressor and activator WOX members oppositely regulate a common downstream target to function in leaf blade outgrowth, offering a novel insight into the role of local cytokinins in balancing cell proliferation and differentiation during lateral organ development.
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Abstract -
Summary Plant lateral organ development is a complex process involving both transcriptional activation and repression mechanisms. The
WOX transcriptional repressorWOX 1/STF , theLEUNIG (LUG ) transcriptional corepressor and theANGUSTIFOLIA 3 (AN 3) transcriptional coactivator play important roles in leaf blade outgrowth and flower development, but how these factors coordinate their activities remains unclear. Here we report physical and genetic interactions among these key regulators of leaf and flower development.We developed a novel
in planta transcriptional activation/repression assay and suggest thatLUG could function as a transcriptional coactivator during leaf blade development.Mt
LUG physically interacts with MtAN 3, and this interaction appears to be required for leaf and flower development. A single amino acid substitution at position 61 in theSNH domain of MtAN 3 protein abolishes its interaction with MtLUG , and its transactivation activity and biological function. Mutations inlug andan3 enhanced each other's mutant phenotypes. Both thelug and thean3 mutations enhanced thewox1 prs leaf and flower phenotypes inArabidopsis .Our findings together suggest that transcriptional repression and activation mediated by the
WOX ,LUG andAN 3 regulators function in concert to promote leaf and flower development, providing novel mechanistic insights into the complex regulation of plant lateral organ development. -
Summary The formation of nitrogen‐fixing nodules on legume hosts is a finely tuned process involving many components of both symbiotic partners. Production of the exopolysaccharide succinoglycan by the nitrogen‐fixing bacterium
Sinorhizobium meliloti 1021 is needed for an effective symbiosis withMedicago spp., and the succinyl modification to this polysaccharide is critical. However, it is not known when succinoglycan intervenes in the symbiotic process, and it is not known whether the plant lysin‐motif receptor‐like kinase MtLYK10 intervenes in recognition of succinoglycan, as might be inferred from work on theLotus japonicus MtLYK10 ortholog, LjEPR3. We studied the symbiotic infection phenotypes ofS. meliloti mutants deficient in succinoglycan production or producing modified succinoglycan, in wild‐typeMedicago truncatula plants and inMtlyk10 mutant plants. On wild‐type plants,S. meliloti strains producing no succinoglycan or only unsuccinylated succinoglycan still induced nodule primordia and epidermal infections, but further progression of the symbiotic process was blocked. TheseS. meliloti mutants induced a more severe infection phenotype onMtlyk10 mutant plants. Nodulation by succinoglycan‐defective strains was achieved byin trans rescue with a Nod factor‐deficientS. meliloti mutant. While the Nod factor‐deficient strain was always more abundant inside nodules, the succinoglycan‐deficient strain was more efficient than the strain producing only unsuccinylated succinoglycan. Together, these data show that succinylated succinoglycan is essential for infection thread formation inM. truncatula , and that MtLYK10 plays an important, but different role in this symbiotic process. These data also suggest that succinoglycan is more important than Nod factors for bacterial survival inside nodules. -
Summary In species with compound leaves, the positions of leaflet primordium initiation are associated with local peaks of auxin accumulation. However, the role of auxin during the late developmental stages and outgrowth of compound leaves remains largely unknown.
Using genome resequencing approaches, we identified insertion sites at four alleles of the
LATERAL LEAFLET SUPPRESSION1 (LLS1 ) gene, encoding the auxin biosynthetic enzyme YUCCA1 inMedicago truncatula .Linkage analysis and complementation tests showed that the
lls1 mutant phenotypes were caused by theTnt1 insertions that disrupted theLLS1 gene. The transcripts ofLLS1 can be detected in primordia at early stages of leaf initiation and later in the basal regions of leaflets, and finally in vein tissues at late leaf developmental stages. Vein numbers and auxin content are reduced in thells1‐1 mutant. Analysis of thells1 sgl1 andlls1 palm1 double mutants revealed thatSGL1 is epistatic toLLS1 , andLLS1 works withPALM1 in an independent pathway to regulate the growth of lateral leaflets.Our work demonstrates that the YUCCA1/YUCCA4 subgroup plays very important roles in the outgrowth of lateral leaflets during compound leaf development of
M. truncatula , in addition to leaf venation.