Shared and unique responses of plants to multiple individual stresses and stress combinations: physiological and molecular mechanisms

Abstract

In field conditions, plants are often simultaneously exposed to multiple biotic and abiotic stresses resulting in substantial yield loss. Plants have evolved various physiological and molecular adaptations to protect themselves under stress combinations. Emerging evidences suggest that plant responses to a combination of stresses are unique from individual stress responses. In addition, plants exhibit shared responses which are common to individual stresses and stress combination. In this review, we provide an update on the current understanding of both unique and shared responses. Specific focus of this review is on heat-drought stress as a major abiotic stress combination and, drought-pathogen and heat-pathogen as examples of abiotic-biotic stress combinations. We also comprehend the current understanding of molecular mechanisms of cross talk in relation to shared and unique molecular responses for plant survival under stress combinations. Thus, the knowledge of shared responses of plants from individual stress studies and stress combinations can be utilized to develop varieties with broad spectrum stress tolerance.

Keywords: concurrent stress; drought; heat; pathogen infection; tailored response; unique adaptation mechanisms.

Figure 1

Representation of unique and shared responses and the “dominant stressor” concept in A. thaliana, T. aestivum, and S. bicolor under combined heat and drought stress. (A) H, D, and C denote the number of genes modulated (refer to both up- and down-regulated) exclusively under heat, drought, and combined heat and drought stress, respectively. HD, HC, DC, and HDC represent the commonly regulated genes under heat and drought stress, heat and combined, drought and combined stresses, and all the three stresses, respectively. The figure is a graphical representation of the data (number of genes modulated under the different stress condition) provided in three independent cDNA array studies in A. thaliana, T. aestivum, and S. bicolor by Rizhsky et al. (2004), Aprile et al. (2013), and Johnson et al. (2014), respectively. (B) Representation of the “dominant stressor concept” under combined stress. The rectangles represent heat and drought stress. In a given stress combination, two stresses involved differ in severity of impact on plants. The severity of the two stresses is represented by “see saw.” In case of A. thaliana, the molecular responses seen are drought specific with a maximum overlap between genes modulated under drought and combined stress. In T. aestivum, the number of heat stress specific genes outweighs the number of drought specific genes. However, the number of combined stress-specific genes is far greater than the individual stress specific genes and molecular response to the combined stress conditions is mostly unique in this plant. In case of S. bicolor, the number of genes specific to heat stress outweighs the number of drought stress specific genes. The genes commonly modulated (both up- and down-regulated) under heat and combined stress forms the maximum share in the combined stress response. H, heat; D, drought; C, combined stress. The pie chart represents the molecular response of plants to the combined stress and the area denotes the number of genes modulated under each category.

Figure 2

Unique and shared responses and the “dominant stressor” concept in A. thaliana under combined heat, virus, and drought stress. (A) Representation of unique and shared responses of A. thaliana under drought, virus infection, and their combination(left) and heat, virus, and their combination (right). The bar diagram (left) represents the number of genes modulated exclusively under virus (V), drought (D), combined heat and drought stress (C) as well as the number of commonly regulated genes under virus infection and drought stress (DV), drought and combined (DC), virus and combined stresses (VC), and all the three stresses (CDV). The bar diagram at the right represents the number of unique genes modulated exclusively under virus (V), heat (H), combined heat and virus stress (C) as well as the number of genes commonly regulated under heat and virus infection (HV), heat and combined (CH), virus and combined stresses (CV), and all the three stresses (CHV). (B) The figure represents the dominant stressor concept. Drought and virus stress are represented by orange and blue rectangles. In this case, virus infection has more effect on the gene expression of A. thaliana plants. The number of genes unique to combined stress is far greater than that of individual stress genes and molecular response to the combined stress conditions is mostly unique. Heat and virus stress are represented by yellow and blue rectangles. In this case, heat stress has more effect on the gene expression. The number of heat and combined stress genes are nearly same and molecular response to the combined stress conditions mostly consists of genes commonly modulated under heat and combined stress. The figure is a graphical representation of the data provided in microarray study by Prasch and Sonnewald (2013). H, heat; D, drought; C, combined stress.

Figure 3

Model representing cross talk between drought and pathogen stress signaling pathway from individual stress studies and its relation to shared and unique response pathway provoked under combined stress. The two inverted triangles in the upper panel represents the drought stress (A) and biotic stress signaling pathway (B) consisting of signal perception, signal transduction, gene expression and response generation steps with the representative gene products. The inverted shape represents the general response (wide upper side) at the stress perception and signal transduction stage culminating to a specific response (tapering lower end) contributing to tolerance to a particular stress. The response of the plants to combined drought and pathogen stress consist of both the shared (responses common to drought and pathogen stress) and unique responses as represented by the triangle (C). The overall response of plants to the combined stress is governed by the key players involving ROS, Ca²⁺, MAPKs, and the different transcription factors as well as some unique genes regulating the tailored responses. The shared responses can be deciphered by understanding the cross talk between the drought and the pathogen stress tolerance signaling networks whereas dedicated studies are required to understand the unique responses. The yellow colored small triangle represents the responses shared between drought and combined stress whereas the blue triangle represents the responses shared between pathogen and combined stress. The overlapping area between the two small triangles represents the responses shared by the drought and pathogen stress. The red colored triangle at the apex represents the unique response under the combined stress. The blue and yellow color spheres represent the calcium and ROS molecules. The red color arrow represents the MAPK pathway. The dashed arrows indicate the cross talk wherein the red colored dashed arrows represent the suppression and blue dashed arrows represent the activation of the respective stress responsive genes. PM, plasma membrane; ABA, abscisic acid; SA, salicylic acid; JA, jasmonic acid; ET, ethylene; M, MAPK pathway; ABA dep, ABA dependent pathway; ABA indep, ABA independent pathway; DREB, dehydration responsive element binding; NAC, NAM-ATAF and CUC 6 transcription factor; ABF, ABA binding factor; AREB, ABA responsive element binding; Myb, myeloblastosis; Myc, myelocytomatosis; ERF, ethylene responsive factor; WRKY stands for the first four amino acids (tryptophan [W], arginine [R], lysine [K], and tyrosine [Y] of the heptapeptide WRKYGQK, which is the hall mark of WRKY proteins; COI1, coronatine insensitive 1; LEA, late embryogenesis; Gly, glyoxylase; dehyd, Dehydrin; PR, pathogenesis related; ROS, reactive oxygen species.