Plant signaling in biotic and abiotic stress

Our planet’s climate is changing, and with it the growth conditions of the crops and animals we depend upon. These changes threaten our food supply, necessitating both understanding and informed action on our side. Conditions such as heat or cold waves, drought, or flooding directly impact the growth of crops, as well as alter their interactions with pathogens. In addition, some of these changes can occur simultaneously, resulting in devastating impacts to our economy. How we prepare for such changes and attempt to mitigate their impact directly depends on our understanding of the basic mechanisms underlying the interaction of plants with different biotic and abiotic stresses, as well as their combination. The history of plant research has demonstrated that understanding and manipulating signal transduction events that occur during early stages of a plant’s interaction with its abiotic or biotic environment can lead to the development of crops with enhanced tolerance to these environmental stresses. For instance, identifying and manipulating a transcription factor (TF) or another regulatory protein that functions early in a defense or acclimation response regulon will often make plants much more tolerant to stress than manipulating one enzyme or one protein that is part of that regulon (e.g., Mittler and Blumwald, 2010; Bailey-Serres et al., 2019). Clearly, this strategy requires basic research to identify these key regulators and their corresponding function(s) within their regulatory nodes. As we look to the future, however, an important concern is that we do not fully understand how individual regulatory nodes may interact with each other to cause beneficial or undesirable outcomes under more complex combinatorial conditions or stresses. To manipulate pathways and networks and to achieve the best outcome(s), we therefore need to understand how each pathway and network function and how they interact with each other. Within plants, numerous signal transduction pathways and networks interact in response to a given biotic or abiotic stimulus. These responses are intertwined with interactions of numerous plant hormones, calcium, and different reactive oxygen species (ROS), as well as a plethora of receptors, kinases, phosphatases, and other regulatory proteins, compounds, and small molecules (e.g. Sierla et al., 2016; Nimma et al., 2017; Gronnier et al., 2018; Kudla et al., 2018; Singh and Chamovitz, 2019; Williams et al., 2019). Each signaling mechanism or network could be influenced by different biotic or abiotic conditions that will alter its overall outcome and affect acclimation to different conditions. However, at present, we understand relatively little about how one pathway impinges on the activity of another. To address this complexity, a conference on Plant Signaling in Biotic and Abiotic Stress was organized at the Christopher S. Bond Life Sciences Center on the Columbia campus of the University of Missouri from 29 to 31 May, 2019 (sponsored by the Interdisciplinary Plant Group). The current special issue summarizes some of the main concepts discussed. Topics covered in this special issue include signaling during abiotic and biotic stresses as it links to development, nutrient availability, and interactions with soil bacteria (Hoang et al., 2020; Matthes et al., 2020; Schwarz and Bauer, 2020). Also discussed are the interactions of stress-related signaling pathways with the perception of light quality (Liscum et al., 2020), as well as with water availability (Dubois and Inzé, 2020). Two additional growing fields in plant stress biology covered are the role of the endoplasmic reticulum (ER) and autophagy in stress signaling (Afrin et al., 2020; Liao and Bassham, 2020), and the response of plants to a combination of two or more stress conditions (Zandalinas et al., 2020). Finally, the relationship(s) between receptor-like kinase signaling and heterotrimeric G-proteins in stress signaling is addressed (Pandey, 2020). Although these reviews cover only a small fraction of the plant abiotic and biotic signaling field, they address many of the central concepts that relate to balancing and integrating different pathways during stress signaling (Box 1). (A) The multiple factors proposed to affect almost all signal transduction pathways in plants. The outcome of almost any signaling pathway needs to integrate many, if not all, of these factors to generate a context-relevant response that will contribute to the successful survival, growth, and reproduction of the plant. (B) Interaction between different signaling complexes integrating input from multiple factors (e.g. inputs A, B, and C) in different subcellular compartments of the cell is proposed to orchestrate the integration of multiple signals and impact gene expression during the triggering of any given signal transduction pathway. Some of these complexes may physically interact to form supercomplexes that integrate multiple signals. Abbreviations used: ER, endoplasmic reticulum; ROS, reactive oxygen species; TF, transcription factor. Integrating different signals, originating from different subcellular compartments under different conditions to orchestrate and coordinate epigenetic, transcriptional, and post-transcriptional regulatory networks and mechanisms, is thought to require membrane- and non-membrane-bound complexes comprising many different proteins (e.g. Nimma et al., 2017; Singh and Chamovitz, 2019; Williams et al., 2019). At present, our understanding of these massive regulatory complexes is rather rudimentary. However, considering the numerous and diverse input signals a plant needs to integrate (Box 1), it is clear that these regulatory complexes need to interact and communicate with each other to correctly process the information, perhaps by generating supercomplexes. Understanding this higher order of combinatorial complexity is a major challenge for our current and future scientific research. Abiotic and/or biotic stress combinations (i.e. the study of how plants respond to two or more different environmental stressors that impact them simultaneously) is a rapidly developing field in plant biology (highlighted in this issue by Zandalinas et al., 2020). It is perhaps one of the best examples for the concept of signal transduction integration. We know much about the pathways and complexes that function in the response of plants to drought, or heat, or high light stresses; but what happens when these stresses interact and impact the plant simultaneously, as can very easily happen in the field? One possible way in which plants may integrate the different signals could be the combinatorial function of different transcriptional networks that use multiple types of TF family members, such as heat shock TFs, MYBs, DREBs, and others (Zandalinas et al., 2020). Different stresses may also be integrated through convergence on basic physiological functions (e.g. photosynthesis, respiration, water, and ion relations), or metabolism (e.g. by affecting fluxes, membrane properties, and enzyme kinetics). From the many examples of stress combination studies highlighted by Zandalinas et al. (2020), it is clear that the combination of two or more different stresses results in a novel transcriptomic signature that contains elements of the response of plants to each of the individual stresses, as well as new transcriptomic responses (sometimes comprising thousands of transcripts) that are unique to the state of stress combination (Zandalinas et al., 2020). The signals generated by each of the different stress conditions must, therefore, have integrated to generate a new type of response to the stress combination. Although the complexity of signal integration generated during multiple stresses may at first appear to be an extreme example, thinking more broadly, a plant’s response to any type of stress requires a high degree of signal integration (Box 1). The plant’s developmental stage and its overall physiological health are ever-changing factors that will alter how a plant responds in an efficient manner to any type of stress. The response to drought stress could, for example, be very different depending on the developmental stage of the plant, its age and physiological status, or the tissue(s) being examined. Additional variables include the composition of soil microbes and proximity of other plants within the plant ecosystem, underscoring the plant’s need for constant signal integration (Box 1). If we accept the number of variables that we take for granted, we realize that, as researchers, we need to change the way we design experiments—or at least to acknowledge the limitations of our approaches. Most scientists are reductionists by training, learning to carefully control specific conditions to obtain highly reproducible responses. While this type of design has been important to identify components of individual pathways, the obvious limitation is that we risk building incomplete models that assume a plant regulates these components in a similar way under all conditions. As a research community, we need to embrace the importance of exploring the more complex ‘real world’. Accepting this open mindset, we can be open to the possibility that the variability or plasticity in the response of plants to different environmental conditions may be providing us with very important information about the complexities of signal integration. There is still so much for us to learn about plant signaling, so, let’s keep working at it. This work was supported by funding from the Interdisciplinary Plant Group, the National Science Foundation (IOS-1923779, IOS-1353886, MCB-1936590, IOS-1932639), and the University of Missouri.