Abstract
Legumes utilize a shoot-mediated signaling system to maintain a mutualistic relationship with nitrogen-fixing bacteria in root nodules. In Lotus japonicus, shoot-to-root transfer of microRNA miR2111 that targets TOO MUCH LOVE, a nodulation suppressor in roots, has been proposed to explain the mechanism underlying nodulation control from shoots. However, the role of shoot-accumulating miR2111s for the systemic regulation of nodulation was not clearly shown. Here, we find L. japonicus has seven miR2111 loci, including those mapped through RNA-seq. MIR2111-5 expression in leaves is the highest among miR2111 loci and repressed after rhizobial infection depending on a shoot-acting HYPERNODULATION ABERRANT ROOT FORMATION1 (HAR1) receptor. MIR2111-5 knockout mutants show significantly decreased nodule numbers and miR2111 levels. Furthermore, grafting experiments using transformants demonstrate scions with altered miR2111 levels influence nodule numbers in rootstocks in a dose-dependent manner. Therefore, miR2111 accumulation in leaves through MIR2111-5 expression is required for HAR1-dependent systemic optimization of nodule number.
Highlights
Legumes utilize a shoot-mediated signaling system to maintain a mutualistic relationship with nitrogen-fixing bacteria in root nodules
We investigated the functions of miR2111 genes in the shoot-mediated nodulation control system known as autoregulation of nodulation (AON), focusing, in particular, on MIR2111-5 locus
L. japonicus possesses at least seven miR2111 genes, including those we identified and four genes expressed in leaves (Fig. 1 and Supplementary Fig. 1a, b)
Summary
Legumes utilize a shoot-mediated signaling system to maintain a mutualistic relationship with nitrogen-fixing bacteria in root nodules. MiR2111 accumulation in leaves through MIR2111-5 expression is required for HAR1-dependent systemic optimization of nodule number Land plants ensure their continuous growth under fluctuating conditions by sharing environmental information between the leaves and roots. Information about light conditions for the leaves[1] and nitrogen (N) deficiency in the roots[2] is transferred using a long-distance communication system[3] These shoot–root communications are accomplished delivering signaling molecules between shoot and roots, such as proteins[1], peptides[2,4,5,6], phytohormones[7,8,9], and RNA species[10,11,12], which are produced locally, in response to various environmental cues. To optimize the number of nodules, legumes utilize a long-distance negative-feedback mechanism known as autoregulation of nodulation (AON)[17]
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