Systemic Optimization of Legume Nodulation: A Shoot-Derived Regulator, miR2111.

Nao Okuma,Masayoshi Kawaguchi

doi:10.3389/fpls.2021.682486

Abstract

Long-distance signaling between the shoot and roots of land plants plays a crucial role in ensuring their growth and development in a fluctuating environment, such as with soil nutrient deficiencies. MicroRNAs (miRNAs) are considered to contribute to such environmental adaptation via long-distance signaling since several miRNAs are transported between the shoot and roots in response to various soil nutrient changes. Leguminous plants adopt a shoot-mediated long-distance signaling system to maintain their mutualism with symbiotic nitrogen-fixing rhizobia by optimizing the number of symbiotic organs and root nodules. Recently, the involvement and importance of shoot-derived miR2111 in regulating nodule numbers have become evident. Shoot-derived miR2111 can systemically enhance rhizobial infection, and its accumulation is quickly suppressed in response to rhizobial inoculation and high-concentration nitrate application. In this mini-review, we briefly summarize the recent progress on the systemic optimization of nodulation in response to external environments, with a focus on systemic regulation via miR2111.

Highlights

Long-distance communication between the shoot and roots of land plants is crucial for coordinating growth and development in fluctuating environments such as soil nutrient deprivation at the whole-plant level (Ko and Helariutta, 2017)
In L. japonicus, M. truncatula, and soybean, miR2111 targets TOO MUCH LOVE (TML)(s) mRNA and can enhance rhizobial infection. miR2111 overexpressing transgenic plants typically exhibit a hypernodulation phenotype. In both leaves and roots, mature miR2111 accumulation and the expression of several miR2111 genes are immediately suppressed in response to rhizobial inoculation and nitrate treatment depending on shoot-acting leucinerich repeat receptor-like kinase (LRR-RLK), such as HYPERNODULATION ABERRANT ROOT1 (HAR1) in L. japonicus, SUPER NUMERIC NODULES (SUNN) in M. truncatula, and NODULE AUTOREGULATION RECEPTOR KINASE (NARK) in soybean
LOTUS HISTIDINE KINASE1 (LHK1) might locally influence TML expression in roots, independent of shoot-acting receptors such as HAR1/ SUNN/NARK (Figure 1)

Summary

INTRODUCTION

Long-distance communication between the shoot and roots of land plants is crucial for coordinating growth and development in fluctuating environments such as soil nutrient deprivation at the whole-plant level (Ko and Helariutta, 2017). Legumes maintain symbiosis with nitrogen-fixing bacteria, known as the rhizobia, in their roots through shootmediated long-distance signaling systems (Caetano-Anollés and Gresshoff, 1991; Ferguson et al, 2019; Gautrat et al, 2020b). Rhizobia can inhabit the nodules and fix atmospheric dinitrogen gas to produce ammonium ions, a plant-available form of nitrogen To maintain this symbiosis, host plants must use photosynthates as energy for nodule formation and bacterial maintenance. Host plants must balance the benefits of nitrogen nutrition provided by rhizobia and the costs of carbon sources for nodulation To optimize this symbiosis, legumes control nodule numbers using long-distance negative/positive feedback systems in response to rhizobial infection and soil nutrient availability (Caetano-Anollés and Gresshoff, 1991; Ferguson et al, 2019). We summarize recent advances in the study of systemic regulation of nodulation in response to external environmental stimuli, focusing on the relevance of shoot-derived miR2111

MOLECULAR BASIS OF AUTOREGULATION OF NODULATION

POSITIVE REGULATION OF

ADAPTATIONS TO PHOSPHATE DEFICIENCY THROUGH AON

Findings

FUTURE PERSPECTIVE