The miR172/IDS1 signaling module confers salt tolerance through maintaining ROS homeostasis in cereal crops

Abstract

Salt stress triggers the overdose accumulation of reactive oxygen species (ROS) in crop plants, leading to severe oxidative damage to living tissues. MicroRNAs (miRNAs) act as master regulators orchestrating the stress responsive regulatory networks as well as salt tolerance. However, the fundamental roles of miRNAs in modulating salt tolerance in cereal crops, especially in salt-triggered ROS scavenging remain largely unknown. Through small RNA sequencing, a salt-responsive miRNA, miR172 was identified in rice. Further, by generating the miR172-overexpression or MIR172 gene loss-of-function mutant lines, the biological significance of miR172 and its downstream signaling pathways related to salt tolerance were defined. We demonstrated that miR172 is a positive regulator of salt tolerance in both rice and wheat. More interestingly, miR172a and miR172b, but not miR172c or miR172d are involved in salt stress response, emphasizing the functional differentiation within miR172 family members. Further evidence uncovers a novel miR172/IDS1 regulatory module that functions as a crucial molecular rheostat in maintaining ROS homeostasis during salt stress, mainly through balancing the expression of a group of ROS-scavenging genes. Our findings establish a direct molecular link between miRNAs and detoxification response in cereal crops for improving salt tolerance.

Comprehensive In Silico Characterization and Expression Profiling of TCP Gene Family in Rapeseed

“…The overexpression of soybean miR172c improves tolerance to drought and salinity stress, and it also enhances sensitivity to ABA in transgenic A. thaliana plants ( Li et al, 2016 ). Recently, Cheng et al (2021) found that miR172s (mainly miR172a and miR172b) act as a positive regulator of salt tolerance in rice and wheat. Further, it also maintains the ROS homeostasis during salt stress, generally by balancing the expression of several ROS-scavenging-related genes in both wheat and rice ( Cheng et al, 2021 ).…”

“…Recently, Cheng et al (2021) found that miR172s (mainly miR172a and miR172b) act as a positive regulator of salt tolerance in rice and wheat. Further, it also maintains the ROS homeostasis during salt stress, generally by balancing the expression of several ROS-scavenging-related genes in both wheat and rice ( Cheng et al, 2021 ). The transgenic B. napus plants overexpressing miR395 indicated a lower degree of cadmium-induced oxidative stress compared to wild-type plants ( Zhang et al, 2013 ).…”

Regulatory short RNAs: A decade's tale for manipulating salt tolerance in plants

“…In rice, the Osa‐ mir172 / IDS1 ( INDETERMINATE SPIKELET1 ) module plays a key role in maintaining ROS homeostasis under salt stress by deregulating the expression of multiple genes encoding detoxification enzymes. The mir172/IDS1 module is also conserved in the cereals and regulates the expression of TaAPX2/5/7/8 , TaGPX1/2/3 , and TaCAT2/4 in wheat (Cheng et al, 2021). In contrast, Arabidopsis lines overexpressing ghrmiR414c exhibited reduced seed germination, seedling biomass, and primary root elongation under salt stress due to the down‐regulation of its target GhFSD , which encodes a Fe‐SOD (Wang et al, 2019).…”

CRISPR‐Cas9 mediated OsMIR168a knockout reveals its pleiotropy in rice

“…CRISPR-Cas based genome editing technology presents a powerful genetic knockout approach to study the function of coding genes and non-coding genes in plants (Bi et al, 2020;Cheng et al, 2021;Liu et al, 2020a;Miao et al, 2019Miao et al, , 2020Ren et al, 2019Ren et al, , 2021Tang et al, 2019;Wang et al, 2019;Zhong et al, 2019Zhong et al, , 2020Zhou et al, 2021). Previously, we successfully applied CRISPR-Cas9 to knock out multiple miRNAs in rice, which provided multiple insights in miRNA genesis and complex regulation (Zhou et al, 2017).…”