Drought attenuates plant responses to multiple rhizospheric pathogens: A study on a dry root rot-associated disease complex in chickpea fields

Abstract

Root rots, a major factor contributing to yield loss in chickpea, often occur in disease complexes. Plant responses to disease complexes are not well elucidated. We sought a clear understanding of a newly identified disease complex in chickpea, dry root rot (DRR)–wilt disease complex, in the field and studied the effect of drought on the severity of the complex and its effect on yield. We compared plant responses to DRR alone and the disease complex under drought and determined the phytohormones involved in plant defense against the disease complex. We compared the effect of 14 environments (two soil moisture regimes at seven locations) on the incidence of the disease complex and yield loss in four chickpea genotypes. We also studied the effect of drought on rhizospheric and root endo-microbial communities by whole-genome and metagenomic sequencing and performed LC-MS-based phytohormonal profiling of chickpea roots. Soil moisture and plant genetic variability were critical in modulating disease incidence in field conditions. DRR was the primary driver of the disease complex under drought stress. Drought aggravated the yield reductions caused by the disease complex from 35% to 60% in susceptible genotypes. Further, drought-tolerant genotypes performed better under combined disease complex infection and drought stress and exhibited lesser yield losses than susceptible genotypes. Pathogenic fungi such as Macrophomina phaseolina, Fusarium oxysporum, and Rhizoctonia solani were enriched in the chickpea rhizosphere, and M. phaseolina was predominant in infected chickpea roots under both well-watered and drought conditions. Symbiotic associations of chickpea with nitrogen-fixing bacteria were suppressed under drought stress. Abscisic acid, jasmonic acid, and salicylic acid were found to be involved in defense against the disease complex across various stages of plant growth. We highlight the interaction between drought and soil pathogens affecting chickpea yield and suggest the utilization of drought-tolerant root traits as donor traits for improving combined stress resistance. We also demonstrate growth stage–dependent phytohormonal responses elicited by DRR and the DRR–wilt disease complex. The identification and management of root rots is essential, and our findings offer valuable new insights into a lesser-known but highly significant disease complex of chickpea. Manuscript data is available at Supplementary File S1. The soil microbe whole-genome and metagenome and root-microbe 16 S and ITS sequencing data are available at NCBI PRJNA871091 and PRJNA895851.