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Genetic regulation of flowering time in annual and perennial plants

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Flowering time plays a significant role in the reproductive success of plants. So far, five major pathways to flowering have been characterized in Arabidopsis, including environmental induction through photoperiod, vernalization, and gibberellins and autonomous floral iation, and aging by sequentially operating miRNAs (typically miR156 and miR172) responding to endogenous cues. The balance of signals from these pathways is integrated by a common set of genes (FLOWERING LOCUS C, FLOWERING LOCUS T, LEAFY, and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1) that determine the flowering time. Recent studies have indicated that epigenetic modification, alternative splicing, antisense RNA and chromatin silencing regulatory mechanisms play an important role in this process by regulating related flowering gene expression. In this review, we discuss the current understanding in genetic regulation of the phase transition from vegetative to reproductive growth by using Arabidopsis as a model. We also describe how this knowledge has been successfully applied for identifying homologous genes from perennial crops. Furthermore, detailed analysis of the similarities and differences between annual and perennial plants flowering will help elucidate the mechanisms of perennial plant maturation and regulation of floral initiation. This article is categorized under: RNA in Disease and Development > RNA in Development

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Outline of flowering pathways in Arabidopsis. A simplified diagram showing the various pathways of flower induction in Arabidopsis based on Andrés and Coupland[18], Zhu and Helliwell[97], and Ietswaart and colleagues [30]. So far, five independent pathways have been identified: vernalization, photoperiod, autonomous, gibberellin, and aging. Floral initiation in Arabidopsis occurs through these pathways. The function of the autonomous and vernalization pathways is to repress the activity of FLC, a repressor of flowering, via chromatin modifications of the FLC locus. The targets of repression by FLC are FT and SOC1, also known as floral pathway integrators, which are positively regulated by the photoperiod pathway. In addition, two long noncoding RNAs (lncRNAs COOLAIR and COLDAIR) are involved in the regulation of FLC. Environmental inputs integrated by FT and SOC1 hubs induce expression of meristem identity regulators (LFY, AP1, AG, and SEP) to start flower formation. The recently identified aging pathway affects flowering time in two ways; first, it represses the activity of repressors of flowering, allowing plants to respond to flowering stimuli, secondly, it directly regulates the floral pathway integrators and meristem identity regulators. The aging pathway and gibberellin pathway accompany with the miRNA (miR156 and miR172) activity.
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Regulation of phase change in Arabidopsis by the aging pathway [61–63, 68, 74, 97]. During early development, the levels of miR156 are initially high, promoting the juvenile vegetative growth phase. As the plant reaches the adult stage, the levels of miR156 steadily decrease, allowing for the production of SPL9 and SPL10 proteins that promote adult leaf traits. At the same time, SPL9 and SPL10 directly induce the expression of miR172. Increased levels of miR172 result in the down‐regulation of six AP2‐like transcription factors that normally repress flowering. Release from this repression, in combination with the flower‐promoting actions of SPL3, SPL4, and SPL5, makes the plant competent to flower and the transition to flowering can occur. Both AP2 and miR172 participate in establishing a sharp boundary between the vegetative outer organs and the inner whorls of reproductive organs. In addition, the T6P pathway controls expression of SPL3, SPL4, and SPL5 in the SAM, partly via miR156 and partly independent of the miR156‐dependent aging pathway.
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