Abstract
Micro-RNAs from legume plants are emerging as relevant regulators of the rhizobia nitrogen-fixing symbiosis. In this work we functionally characterized the role of the node conformed by micro-RNA319 (miR319) – TEOSINTE BRANCHED/CYCLOIDEA/PCF (TCP) transcription factor in the common bean (Phaseolus vulgaris) – Rhizobium tropici symbiosis. The miR319d, one of nine miR319 isoforms from common bean, was highly expressed in root and nodules from inoculated plants as compared to roots from fertilized plants. The miR319d targets TCP10 (Phvul.005G067950), identified by degradome analysis, whose expression showed a negative correlation with miR319d expression. The phenotypic analysis of R. tropici-inoculated composite plants with transgenic roots/nodules overexpressing or silencing the function of miR319d demonstrated the relevant role of the miR319d/TCP10 node in the common bean rhizobia symbiosis. Increased miR319d resulted in reduced root length/width ratio, increased rhizobial infection evidenced by more deformed root hairs and infection threads, and decreased nodule formation and nitrogenase activity per plant. In addition, these plants with lower TCP10 levels showed decreased expression level of the jasmonic acid (JA) biosynthetic gene: LOX2. The transcription of LOX2 by TCPs has been demonstrated for Arabidopsis and in several plants LOX2 level and JA content have been associate with TCP levels. On this basis, we propose that in roots/nodules of inoculated common bean plants TCP10 could be the transcriptional regulator of LOX2 and the miR319d/TCP10 node could affect nodulation through JA signaling. However, given the complexity of nodulation, the participation of other signaling pathways in the phenotypes observed cannot be ruled out.
Highlights
Legumes are ecologically important because of their ability to establish an efficient symbiotic association with nitrogen-fixing rhizobia, resulting in the formation of root nodules, where rhizobia can fix the atmospheric dinitrogen (N2) in forms that can be assimilated by the plant, in exchange for a carbon source
Small RNAs differentially expressed during nodule organogenesis have been identified in different legumes such as Medicago truncatula, soybean (Glycine max), Lotus japonicus and common bean (Lelandais-Brière et al, 2009; De Luis et al, 2012; Turner et al, 2012; Formey et al, 2014, 2015, 2016)
Only few in-depth studies that evidence the role of miRNAs in the rhizobial infection, nodulation or Symbiotic nitrogen fixation (SNF) processes have been reported
Summary
Legumes are ecologically important because of their ability to establish an efficient symbiotic association with nitrogen-fixing rhizobia, resulting in the formation of root nodules, where rhizobia can fix the atmospheric dinitrogen (N2) in forms that can be assimilated by the plant, in exchange for a carbon source. Symbiotic nitrogen fixation (SNF) reduces the cost of legume cultivation and is relevant for sustainable agriculture (Venkateshwaran et al, 2013) The evolution of this symbiosis was a key to success for the legume family that comprises 18,000 described species miR319d/TCP10 Regulates Nodulation with approximately 700 genera and represents one-third of the primary crop production in the world; legume production necessary for feed and food relies on only a few cultivated species (Doyle and Luckow, 2003). Studies based on high-throughput sRNA sequencing have identified miRNA families that are expressed in nodules from different legume species (Subramanian et al, 2008; Lelandais-Brière et al, 2009; De Luis et al, 2012; Turner et al, 2012). In this work we analyzed the role of miR319d from common bean in symbiosis with R. tropici
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