lncRNA7 and lncRNA2 modulate cell wall defense genes to regulate cotton resistance to Verticillium wilt

Authors: ZHANG, LIN - Henan Normal University; CHEN, JIERU - Henan Normal University; LIU, JINLEI - Henan Normal University; SUN, QUAN - Henan Normal University; Liu, Jinggao; LI, HUIMIN - Henan Normal University; WANG, PING - Henan Normal University; CHU, ZONGYAN - Henan University; ZHANG, XIAO - Henan University; YUAN, YOULU - Henan University; SHI, YUZHEN - Henan University; CAI, YINGFAN - Henan University

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/26/2021
Publication Date: 2/3/2022
Citation: Zhang, L., Chen, J., Liu, J., Sun, Q., Liu, J., Li, H., Wang, P., Chu, Z., Zhang, X., Yuan, Y., Shi, Y., Cai, Y. 2022. lncRNA7 and lncRNA2 modulate cell wall defense genes to regulate cotton resistance to Verticillium wilt. Plant Physiology. Article kiac041. https://doi.org/10.1093/plphys/kiac041.
DOI: https://doi.org/10.1093/plphys/kiac041

Interpretive Summary: Verticillium wilt is a major cotton disease caused by the soil dwelling fungus, Verticillium dahliae. Currently, the only economically viable method of controlling this disease is by planting cotton varieties that have some resistance to the disease, but the mechanism(s) of resistance to Verticillium wilt in cotton remains unclear. In this study, we used a molecular technique called RNA-seq to identify genetic elements called lncRNAs that control genes involved in cell wall defense against this disease. One of the elements, lncRNA2, regulates a cell wall degrading protein which leads to decreased Verticillium wilt resistance. Another element, lncRNA7, increased wilt resistance through regulation of a protein that hinders the function of another protein that loosens the cell wall. The regulation of these proteins and cell wall degradation products was found to be controlled by a plant hormone called Indole-3-acetic acid. The identification of these new wilt disease-related lncRNAs and respective target genes involved in cell wall defense will facilitate both traditional breeding and genetic-based efforts to develop wilt resistant cotton varieties.

Technical Abstract: Plant long noncoding RNAs regulate disease resistance against fungi and other pathogens, but the mechanism remains unclear. We identified disease resistance-related new lncRNAs, their target genes and their functions using cotton chromosome segment substitution lines inoculated with Verticillium dahliae. The results showed that the newly discovered lncRNA7 and its target gene pectin methylesterase inhibitor GbPMEI13 positively regulated disease resistance, via silencing approach and ectopic overexpression of GbPMEI13 in Arabidopsis, promoted growth and enhanced resistance to Verticillium dahliae. In contrast, lncRNA2 and its target gene polygalacturonase GbPG12 negatively regulated resistance to Verticillium dahliae. We found that fungal-disease-related agents, oligogalacturonide (OG), which is produced by pectin-breakdown, could down-regulate the expression of lncRNA2, leading to decreased expression of GbPG12, which reduces degradation of pectin. However, OG up-regulated the expression of lncRNA7, which coded a plant peptide hormone phytosulfokine (PSK-a) precursor. PSK-a caused IAA accumulation and activated GbPMEI13 expression with ARF5. Accumulation of GbPMEI13 inhibited GbPME enzyme activity, causing increased methylation of pectin, resulting in increased resistance to Verticillium dahliae. We also demonstrated that GbPMEI13 by itself inhibited the mycelial growth and spore germination of Verticillium dahliae in vitro. We demonstrated that the new lncRNA7, lncRNA2 and their target genes are important regulators associated with cell wall defense mediated by auxin signaling, providing new targets for cotton breeding.