Impact of Combined Abiotic and Biotic Stresses on Plant Growth and Avenues for Crop Improvement by Exploiting Physio-morphological Traits

Abstract

Global warming leads to the concurrence of a number of abiotic and biotic stresses, thus affecting agricultural productivity. Occurrence of abiotic stresses can alter plant-pest interactions by enhancing host plant susceptibility to pathogenic organisms, insects, and by reducing competitive ability with weeds. On the contrary, some pests may alter plant response to abiotic stress factors. Therefore, systematic studies are pivotal to understand the effect of concurrent abiotic and biotic stress conditions on crop productivity. However, to date, a collective database on the occurrence of various stress combinations in agriculturally prominent areas is not available. This review attempts to assemble published information on this topic, with a particular focus on the impact of combined drought and pathogen stresses on crop productivity. In doing so, this review highlights some agriculturally important morpho-physiological traits that can be utilized to identify genotypes with combined stress tolerance. In addition, this review outlines potential role of recent genomic tools in deciphering combined stress tolerance in plants. This review will, therefore, be helpful for agronomists and field pathologists in assessing the impact of the interactions between drought and plant-pathogens on crop performance. Further, the review will be helpful for physiologists and molecular biologists to design agronomically relevant strategies for the development of broad spectrum stress tolerant crops.

Keywords: crop production; drought and pathogen infection; morpho-physiological traits; productivity; stress combinations; stress interaction.

FIGURE 1

Schematic representation of effect of stress combination on plants. (A) Effect of combined stresses on plants is explained by representative examples of heat and drought (abiotic–abiotic stress) and drought and pathogen stress (abiotic–biotic stress) combination. (i) Depending on the nature of stresses, the two stresses can either not interact physically, but individually affect the plant leading to a net negative impact on plant growth or interact at plant interface and cause a net effect on the plant. Generally, abiotic stress combinations are examples of “only net effects and no stress interactions”. For example, simultaneous exposure to heat and salinity leads to enhanced retardation of physiological processes such as photosynthesis. (ii) Stress interactions are conspicuous in abiotic and biotic stress combinations wherein one stress factor affects the other stress factor per se. For example, exposure to combined drought and pathogen stress may result in a complex scenario encompassing an interaction of the two stresses along with the impact of the two stresses on the plant. Depending on the plant patho-system, the interaction may lead to enhanced or reduced susceptibility to a particular pathogen. Some pathogens also modulate drought tolerance of the plant. (B) Effect of multiple individual stresses (sequential stresses) on plants. Sequential stresses may either lead to priming or predisposition of plants to the subsequent stress as explained by examples of heat–pathogen and drought–pathogen stress combinations. (i) Priming: Exposure of plants to moderate heat stress (indicated by red arrow) may prime the plants to the subsequent pathogen infection. Mild stress can evoke stress memory in the form of epigenetic changes or transcriptomic changes in plants which may last short or long-term, leading to enhanced tolerance of stress to subsequent more severe stresses (same or different stress). (ii) Predisposition: A pre-occurring drought stress can pre-dispose plants to pathogen infection due to weakened plant defenses or any other metabolic changes occurring due to the drought stress. 1, Mittler, 2006; 2, Ahmed et al., 2013; 3, Gupta et al., 2016; 4, Sharma and Pande, 2013; 5, Xu et al., 2008; 6, Crisp et al., 2016; 7, Mayek-Perez et al., 2002.

FIGURE 2

Impact of combined abiotic stress and pathogen infection on plants. The impact of combined abiotic stresses (mainly drought) and pathogen infection has been shown by taking examples from a few representative studies. (A) Impact of weather variables like temperature, rainfall and relative humidity (RH) on development of stem rot caused by Sclerotinia sclerotiorum in Cicer arietinum during the year 1993–1994 (Sharma et al., 2012). The figure shows increased incidence of stem rot under conditions of high humidity and high rainfall. (B) Effect of drought on Puccinia recondita infection in T. aestivum. Drought enhanced lesion development (Bethenod et al., 2001). (C) Effect of drought on Erysiphe cruciferarum infection in Alliaria petiolata. Drought and fungal infection had additive effect on plant growth. Drought although slowed disease development (decreased % diseased leaf area under drought conditions), plants under drought stress were much smaller as compared to well watered ones, so the powdery mildew occupied the total leaf area by the end of the experiment (Enright and Cipollini, 2007). (D) Effect of drought on infection by Rhizoctonia bataticola in Cicer arietinum. Drought (corresponding to 40% field capacity) predisposed chickpea to dry root rot (Sharma and Pande, 2013). All the graphs have been reconstructed from data taken from respective studies.

FIGURE 3

Outline of strategies for improving crop performance under combined drought and pathogen stress. For understanding the effect of stress on plants, it is important to first understand the nature of the stress combinations, i.e., the interaction between the two stresses as influenced by the timing, intensity, and duration. For example, the pathogen–drought stress interaction can be understood by studying the effect of drought on pathogen life-cycle and virulence. The net effect can be deciphered by studying the response of plants to combined stress which comprises of shared and unique responses. For example, a comparison of pre-existing information on a plant’s molecular responses to individual stresses (microarray datasets and metabolic profile) can help in the identification of probable shared responses. Unique responses can be studied by performing actual combined stress studies and investigating physiological, molecular, and metabolic changes in plants under the stress combinations. The other area of research can be the identification of traits associated with combined stress tolerance (A). Few strategies are available for improving plant tolerance to combined stress conditions. A comprehensive understanding of the nature and effect of stress combination on plants is helpful in devising effective strategies for crop improvement under combined stress conditions. If the stress interaction is important in defining the disease incidence, strategies exploiting the stress interaction can be more helpful in enhancing tolerance of plants to combined stress. For example, a simple modulation in irrigation regime can help in combating the pathogen infection. If the net effect of both the stresses on plants is more important, the information derived from the transcriptomic studies can be utilized to select candidate genes and plants with better adaptation to combined stress can be engineered by suitable modulation of expression of the candidate genes (B).