Auxin response factors (ARFs) are plant transcription factors that activate or repress the expression of auxin-responsive genes and accordingly, play key roles in auxin-mediated developmental processes. Here we identified and characterized the Solanum lycopersicum (tomato) ARF10 homolog (SlARF10), demonstrated that it is posttranscriptionally regulated by Sl-miR160, and investigated the significance of this regulation for tomato development. In wild-type tomato, SlARF10 is primarily expressed in the pericarp of mature and ripened fruit, showing an expression profile complementary to that of Sl-miR160. Constitutive expression of wild-type SlARF10 did not alter tomato development. However, transgenic tomato plants that constitutively expressed the Sl-miR160a-resistant version (mSlARF10) developed narrow leaflet blades, sepals and petals, and abnormally shaped fruit. During compound leaf development, mSlARF10 accumulation specifically inhibited leaflet blade outgrowth without affecting other auxin-driven processes such as leaflet initiation and lobe formation. Moreover, blade size was inversely correlated with mSlARF10 transcript levels, strongly implying that the SlARF10 protein, which was localized to the nucleus, can function as a transcriptional repressor of leaflet lamina outgrowth. Accordingly, known auxin-responsive genes, which promote cell growth, were downregulated in shoot apices that accumulated increased mSlARF10 levels. Taken together, we propose that repression of SlARF10 by Sl-miR160 is essential for auxin-mediated blade outgrowth and early fruit development.
Being composed of several whorls of distinct floral organs, the flower is one of the most complex organs in the plant. As such, the formation and maintenance of boundaries that separate the meristem from the floral organ primordium and adjacent organs are critical for its normal development. In Arabidopsis, the miR164-regulated NAM genes play key roles in floral-boundary specification. By contrast, much less is known about floral-boundary establishment in the model crop tomato. It was found that the miR164-regulated NAM gene GOBLET is expressed in the floral meristem–organ boundaries and its loss-of-function mutant produces flowers with fused organs, indicating its requirement for tomato floral-boundary formation. It was found here that sly-miR164 targets the transcripts of three additional uncharacterized NAM genes in developing flowers. It is shown that, after floral-boundary initiation, the NAM gene Solyc03g115850 (SlNAM2) is expressed as stripes that mark the boundaries between sepals and between different floral whorls. Furthermore, ectopic accumulation of SlNAM2-encoding transcripts caused various growth-suppression and extraorgan phenotypes typically observed in plants over-expressing known boundary genes. Flower-specific silencing of sly-miR164-targeted NAM genes (AP1>>MIR164) caused defects in the separation of sepals and floral whorls indicating abnormal boundary specification. However, supplementing these NAM-deficient flowers with miR164-resistant SlNAM2 suppressed their fusion phenotypes and completely restored floral boundaries. Together, our results strongly suggest that SlNAM2 participates in the establishment of tomato flower whorl and sepal boundaries.
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