Regulated RNA metabolism appears to be a critical component of molecular mechanisms directing flowering initiation in plants. A group of RNA binding proteins exerts their roles through the autonomous flowering pathway. Posttranscriptional mechanisms regulated by microRNAs (miRNAs) also play a key role in flowering-time control. Here, we demonstrate that the GIGANTEA (GI)-regulated miR172 defines a unique genetic pathway that regulates photoperiodic flowering by inducing FLOWERING LOCUS T (FT) independent of CONSTANS (CO). A late-flowering mutant in which a miR172 target gene, TARGET OF EAT1, is constitutively activated by the nearby insertion of the cauliflower mosaic virus 35S enhancer normally responded to vernalization and gibberellic acid treatments. By contrast, its response to daylength changes was severely disrupted. In the mutant, FT was significantly repressed, but other flowering genes were unaffected. Notably, miR172 abundance is regulated by photoperiod via GI-mediated miRNA processing. Accordingly, miR172-overproducing plants exhibit early flowering under both long days and short days, even in the absence of functional CO, indicating that miR172 promotes photoperiodic flowering through a CO-independent genetic pathway. Therefore, it appears that GI-mediated photoperiodic flowering is governed by the coordinated interaction of two distinct genetic pathways: one mediated via CO and the other mediated via miR172 and its targets.

Plants constantly monitor environmental fluctuations to optimize their growth and metabolism. One example is adaptive growth occurring in response to biotic and abiotic stresses. Here, we demonstrate that GH3-mediated auxin homeostasis is an essential constituent of the complex network of auxin actions that regulates stress adaptation responses in Arabidopsis. Endogenous auxin pool is regulated, at least in part, through negative feedback by a group of auxin-inducible GH3 genes encoding auxin-conjugating enzymes. An Arabidopsis mutant, wes1-D, in which a GH3 gene WES1 is activated by nearby insertion of the 35 S enhancer, exhibited auxin-deficient traits, including reduced growth and altered leaf shape. Interestingly, WES1 is also induced by various stress conditions as well as by salicylic acid and abscisic acid. Accordingly, wes1-D was resistant to both biotic and abiotic stresses, and stress-responsive genes, such as pathogenesis-related genes and CBF genes, were upregulated in this mutant. In contrast, a T-DNA insertional mutant showed reduced stress resistance. We therefore propose that GH3-mediated growth suppression directs reallocation of metabolic resources to resistance establishment and represents the fitness costs of induced resistance.

SUMMARYmiR156 and its target SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) genes constitute an endogenous flowering pathway in Arabidopsis. The SPL genes are regulated post-transcriptionally by miR156, and incorporate endogenous aging signals into floral gene networks. Intriguingly, the SPL genes are also regulated transcriptionally by FLOWERING LOCUS T (FT)-mediated photoperiod signals. However, it is unknown how photoperiod regulates the SPL genes. Here, we show that SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) and FT regulate the SPL3, SPL4 and SPL5 genes by directly binding to the gene promoters in response to photoperiod signals. Notably, the SOC1 regulation of the SPL genes, termed the SOC1-SPL module, also mediates gibberellic acid (GA) signals to promote flowering under non-inductive short days (SDs). Under SDs, the inductive effects of GA on the SPL genes disappeared in the soc1-2 mutant, and the flowering of SPL3-overexpressing transgenic plants (35S:SPL3) was less sensitive to GA. In addition, the 35S:SPL3 · soc1-2 plants flowered much earlier than the soc1-2 mutant, supporting SOC1 regulation of the SPL genes. Our observations indicate that the SOC1-SPL module serves as a molecular link that integrates photoperiod and GA signals to promote flowering in Arabidopsis.

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