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.
Plants continuously form new organs in different developmental contexts in response to environmental cues. Underground lateral roots initiate from prepatterned cells in the main root, but cells can also bypass the root-shoot trajectory separation and generate shoot-borne roots through an unknown mechanism. We mapped tomato (
Solanum lycopersicum
) shoot-borne root development at single-cell resolution and showed that these roots initiate from phloem-associated cells through a unique transition state. This state requires the activity of a transcription factor that we named
SHOOTBORNE ROOTLESS
(
SBRL
)
.
Evolutionary analysis reveals that
SBRL
’s function and cis regulation are conserved in angiosperms and that it arose as an ancient duplication, with paralogs controlling wound-induced and lateral root initiation. We propose that the activation of a common transition state by context-specific regulators underlies the plasticity of plant root systems.
MicroRNA 159 (miR159) is a highly conserved miRNA with roles in flowering under short days, anther development and seed germination via repression of GAMYB-like genes. In tomato, the function of miR159 (Sl-miR159) is currently unknown and target transcripts have not been experimentally validated. Here, we identified and characterized a new miR159 target gene (SGN-U567133) in Solanum lycopersicum (tomato) that is not related to MYB. SGN-U567133 is predominantly expressed in flowers and encodes a nuclear-localized protein that contains a unique NOZZLE-like domain at its N terminus. In tomato, SGN-U567133 represents a small gene family and orthologs have been identified in other plant species, all containing a conserved miR159 target site in their coding sequence. Accordingly, 5'-RACE cleavage assay supported miRNA-mediated cleavage of SGN-U567133 transcripts in vivo. Moreover, the SGN-U567133 transcript accumulated in P19-HA-expressing tomato leaves in which miRNA-mediated cleavage is inhibited. In addition, transgenic tomato plants expressing a miR159-resistant form of SGN-U567133 accumulated higher levels of the SGN-U567133 transcript and exhibited defects in leaf and flower development. Together, our results suggest that SGN-U567133 represents a novel class of miR159 targets in plants and raise the possibility that its post-transcriptional regulation by Sl-miR159 is essential for normal tomato development.
HighlightFunctional analysis of the tomato HAM genes suggest that they are involved in critical meristem functions and play homologous roles in compound leaf development.
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