Update on MicroRNAs in the Rhizobia Legume Symbiosis MicroRNAs in the Rhizobia Legume Symbiosis

Legumes are agronomically valuable crops for food and fodder production worldwide because they are rich in protein, oil, fiber, and micronutrients. In addition, legumes require less chemical fertilizer than other major crop plants since they can assimilate some nutrients through symbiotic interactions with soil microbes. These relationships are mutually beneficial for the partners because the plant provides carbon-based energy to the microbe in exchange for essential nutrients. In permissive environmental conditions, legumes can establish symbiotic interactions with rhizobial bacteria and with arbuscular mycorrhizal (AM) fungi. The rhizobia-legume symbiosis leads to formation of root nodules, the site of bacterial nitrogen fixation, and nitrogen uptake by the host plant, whereas the AM symbiosis results in the formation of arbuscules, the site for phosphorous nutrient exchange. Notably, a wide range of plant hosts can form a mycorrhizal symbioses, as opposed to the rhizobial symbiosis that is nearly exclusive to legumes. Formation of a successful symbiosis is contingent upon a nutritional insufficiency of the plant. In the case of the rhizobialegume symbiosis, the plants form symbiotic root nodules when grown in nitrogen-limiting conditions, but do not initiate the symbiosis when nitrogen levels are adequate. Nitrogen-stressed plants begin a molecular dialogue with rhizosphere microbes, initiating the early stages of symbiosis. Ultimately, changes in plant and bacterial gene expression facilitate microbial infection of the plant root, the development of symbiotic root structures, and the maintenance of nitrogen-fixing root nodules. Plants secrete flavonoids and related compounds from the actively growing region of the root. These compounds promote the expression of nod genes in compatible rhizobial species, and nod-gene products synthesize nod factor, bacterial lipochito-oligosaccharide signaling molecules. Plant perception of nod factors by LysM receptor-like kinase potentiates immediate subcellular changes in the root epidermis and later changes in the root cortex. Root epidermal cells respond by depolarization of the root hair plasma membrane, and cytoplasmic Ca spiking in the root hair initiates a signaling pathway involving a calcium and calmodulin-dependant protein kinase (CaMK), two GRAS family proteins Nodulation Signaling Pathway1 (NSP1) and NSP2, and an ethylene response factor transcription factor, ERN (for ethylene response factor required for nodulation). Cortical cells respond to nod factor signals by reinitiating the cell cycle, forming a nodule meristem. Subsequent to plant responses to nod factor, bacteria invade the plant body (see Ding and Oldroyd, 2009 for a summary of early signaling). Select epidermal cells form infection threads that are plasma membrane-lined conduits of extracellular matrix. Rhizobia invade root through the infection thread by a combination of cell division and tumbling within the thread matrix (Fournier et al., 2008). The threads branch and form though cortex cells, ultimately uniting with cells in the nascent nodule where bacteria are released into the cell cytoplasm in a process resembling endocytosis. Within the host-plant cytoplasm, the bacteria differentiate into nitrogen-fixing bacteroids that exchange bioavailable nitrogen for carbon energy from the host plant. The molecular determinants and regulatory networks involved in symbiotic nodule development and function have not been completely elucidated, although recently there has been remarkable progress. The relatively recent discovery of small RNAs (sRNAs) as important components of plant gene regulation and plant development has initiated questions about their role in the legume symbioses. To date, the functions of sRNAs in legume symbioses have been largely unexplored. However, this area of research is advancing rapidly. The aim of this Update is to summarize the current state of knowledge about legume sRNAs, specificallymicroRNAs (miRNAs), in the rhizobia-legume symbiosis. sRNA regulation in complimentary research areas will also be discussed, including the roles of miRNAs in nutrient balance, plant development, plant microbe interactions, since all of these are essential to the rhizobia-legume symbiosis.