Elevated Temperatures Cause Loss of Seed Set in Common Bean
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Soltani et al. BMC Genomics (2019) 20:312 https://doi.org/10.1186/s12864-019-5669-2 RESEARCH ARTICLE Open Access Elevated temperatures cause loss of seed set in common bean (Phaseolus vulgaris L.) potentially through the disruption of source-sink relationships Ali Soltani1,2* , Sarathi M. Weraduwage3, Thomas D. Sharkey2,3,4 and David B. Lowry1,2 Abstract Background: Climate change models predict more frequent incidents of heat stress worldwide. This trend will contribute to food insecurity, particularly for some of the most vulnerable regions, by limiting the productivity of crops. Despite its great importance, there is a limited understanding of the underlying mechanisms of variation in heat tolerance within plant species. Common bean, Phaseolus vulgaris, is relatively susceptible to heat stress, which is of concern given its critical role in global food security. Here, we evaluated three genotypes of P. vulgaris belonging to kidney market class under heat and control conditions. The Sacramento and NY-105 genotypes were previously reported to be heat tolerant, while Redhawk is heat susceptible. Results: We quantified several morpho-physiological traits for leaves and found that photosynthetic rate, stomatal conductance, and leaf area all increased under elevated temperatures. Leaf area expansion under heat stress was greatest for the most susceptible genotype, Redhawk. To understand gene regulatory responses among the genotypes, total RNA was extracted from the fourth trifoliate leaves for RNA-sequencing. Several genes involved in the protection of PSII (HSP21, ABA4, and LHCB4.3) exhibited increased expression under heat stress, indicating the importance of photoprotection of PSII. Furthermore, expression of the gene SUT2 was reduced in heat. SUT2 is involved in the phloem loading of sucrose and its distal translocation to sinks. We also detected an almost four-fold reduction in the concentration of free hexoses in heat-treated beans. This reduction was more drastic in the susceptible genotype. Conclusions: Overall, our data suggests that while moderate heat stress does not negatively affect photosynthesis, it likely interrupts intricate source-sink relationships. These results collectively suggest a physiological mechanism for why pollen fertility and seed set are negatively impacted by elevated temperatures. Identifying the physiological and transcriptome dynamics of bean genotypes in response to heat stress will likely facilitate the development of varieties that can better tolerate a future of elevated temperatures. Keywords: Heat stress, Common bean, Photosynthesis, Transcriptome, Source-sink relationships * Correspondence: [email protected] 1Department of Plant Biology, Michigan State University, East Lansing, MI, USA 2Plant Resilience Institute, Michigan State University, East Lansing, MI, USA Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Soltani et al. BMC Genomics (2019) 20:312 Page 2 of 18 Background Common bean is an economically important crop that Heat is among the most devastating abiotic stresses nega- originated and was domesticated in the New World. P. tively impacting crop production and food security world- vulgaris is separated into two major genepools: Middle wide [1]. Every 1 °C increase in seasonal temperature American and Andean [23, 24]. Humans domesticated results in a 10–17% reduction in crop yields [2, 3]. With beans from both of these major gene pools independently the global mean temperatures set to increase at a pace of [25]. Further, three major races have been characterized 0.2 °C per decade, the impact of heat on worldwide food within the Middle American genepool: Mesoamerica, production will only become more acute [4]. For some re- Durango, and Jalisco. Similarly, there are three races in gions of the globe, temperatures are increasing even more Andean genepool: Nueva Granada, Chile, and Peru. After rapidly and heat waves are expected to increase in inten- the colonization of the New World, Andean beans were in- sity and duration [5]. troduced to European and African countries [26]. Today, Elevated temperatures negatively affect several crucial beans are cultivated in many regions of the world. However, physiological processes in plants. One of the effects of being adapted to moderate climates [27], common bean elevated temperature is an increased accumulation of re- has limited heat tolerance. Seed yield reductions have been active oxygen species (ROS), [6] which are harmful to reported for temperatures higher than 30 °C during the day plant membranes, proteins, and other macromolecules. or higher than 20 °C at nights [28]. Heat stress-induced Photosynthesis is also affected by elevated temperatures, yield reductions were described as a result of flower abscis- with carbon assimilation reduced as a result of a reduc- sions, development of parthenocarpic pods (pin pods), tion in rubisco activation [7, 8]. Rubisco activase is lower seed set per pod or decreased seed size [28, 29]. The inhibited at high temperature, leading to heat-induced level of heat sensitivity in beans depends strongly on the deactivation of rubisco under moderate heat stress [9, developmental stage in which plants are exposed to ele- 10]. Further, heat modifies cell membrane characteristics vated temperatures. Several studies reported that heat stress and consequently affects membrane-binding proteins at pre-fertilization stages are more detrimental to pollen de- [11–13]. Photosystem II (PSII) is thought to be particu- velopment and/or anther dehiscence [29, 30]. Furthermore, larly sensitive to heat stress. However, negative effects of Shonnard and Gepts [31] reported sensitivity of beans to heat stress on net photosynthesis has not been reported heat stress at pod filling stages in addition to flower bud in all crops [14]. Besides carbon assimilation, carbon formation. translocation from source to sink tissues has been shown Elevated temperatures are predicted to be more to be interrupted by heat stress [15]. Continuous sucrose frequent, particularly in some Central American and transport from source leaves to developing reproductive African countries, where Andean genotypes are the main tissues is crucial for male fertility, seed set, and seed fill- beans in cultivation [32]. Heat and drought stress often ing [16, 17]. Pressman et al. [18] found that the disrup- impact crops simultaneously in these regions. While irri- tion of sucrose supply and/or its breakdown to hexoses gation can be used to eliminate water stress, the direct under heat stress results in male sterility and aborted impacts of heat stress cannot be alleviated by any man- seed set in tomato, a drastic negative impact of this abi- agement practice. Development of heat tolerant varieties otic stress on the carbon balance of a plant. remains the only practical solution for minimizing the Several mechanisms to cope with heat have evolved in negative effects of elevated temperatures. Developing plants. Elevated temperatures triggers a suite of physio- bean varieties that can better tolerate elevated tempera- logical responses that can ameliorate the deleterious ef- tures is now considered crucial in both Latin America fects of heat. For example, the ROS scavenging [33] and Africa [34]. Several heat tolerant varieties have machinery is overexpressed, which will convert ROS to been identified and used in breeding pipelines [31, 33, less harmful molecules [19]. ROS also serves as a signal- 35, 36]. Understanding the differential physiological re- ing molecule that can activate heat shock factors (HSFs), sponses of heat-sensitive and heat-tolerant Andean ge- [20, 21]. HSFs bind to palindromic motifs in the pro- notypes to elevated temperatures is a crucial step toward moter of heat responsive genes, including heat shock improving the thermo-tolerance of this economically im- proteins (HSPs). HSPs are molecular chaperones that re- portant crop. fold and stabilize protein structures under heat stress. Here, we investigate the transcriptome and physiological Besides adopting these thermo-tolerance strategies, pre- responses of three varieties of Andean beans to ele- ventative mechanisms have evolved that improve the vated temperatures. These varieties were selected cooling capacity of the leaves by increasing transpiration based on their tolerance (Sacramento and NY-105) or rates [22]. susceptibility (Redhawk) to heat stress. The main ob- In this study, we focused on understanding how jectives of this study were: i) to elucidate the effect of heat-tolerant and heat-sensitive varieties of the common heat stress on the leaf morpho-physiology of the bean bean, Phaseolus vulgaris, respond to elevated temperatures. plants, ii) understand the transcriptomic responses of Soltani et al. BMC Genomics (2019) 20:312 Page 3 of 18 leaves under elevated temperatures, and iii)toidentify Effect of elevated temperature on seed set the potential genes/physiological