Heat tolerance in plants: An overview

Abstract

Heat stress due to increased temperature is an agricultural problem in many areas in the world. Transitory or constantly high temperatures cause an array of morpho-anatomical, physiological and biochemical changes in plants, which affect plant growth and development and may lead to a drastic reduction in economic yield. The adverse effects of heat stress can be mitigated by developing crop plants with improved thermotolerance using various genetic approaches. For this purpose, however, a thorough understanding of physiological responses of plants to high temperature, mechanisms of heat tolerance and possible strategies for improving crop thermotolerance is imperative. Heat stress affects plant growth throughout its ontogeny, though heat-threshold level varies considerably at different developmental stages. For instance, during seed germination, high temperature may slow down or totally inhibit germination, depending on plant species and the intensity of the stress. At later stages, high temperature may adversely affect photosynthesis, respiration, water relations and membrane stability, and also modulate levels of hormones and primary and secondary metabolites. Furthermore, throughout plant ontogeny, enhanced expression of a variety of heat shock proteins, other stress-related proteins, and production of reactive oxygen species (ROS) constitute major plant responses to heat stress. In order to cope with heat stress, plants implement various mechanisms, including maintenance of membrane stability, scavenging of ROS, production of antioxidants, accumulation and adjustment of compatible solutes, induction of mitogen-activated protein kinase (MAPK) and calcium-dependent protein kinase (CDPK) cascades, and, most importantly, chaperone signaling and transcriptional activation. All these mechanisms, which are regulated at the molecular level, enable plants to thrive under heat stress. Based on a complete understanding of such mechanisms, potential genetic strategies to improve plant heat-stress tolerance include traditional and contemporary molecular breeding protocols and transgenic approaches. While there are a few examples of plants with improved heat tolerance through the use of traditional breeding protocols, the success of genetic transformation approach has been thus far limited. The latter is due to limited knowledge and availability of genes with known effects on plant heat-stress tolerance, though these may not be insurmountable in future. In addition to genetic approaches, crop heat tolerance can be enhanced by preconditioning of plants under different environmental stresses or exogenous application of osmoprotectants such as glycinebetaine and proline. Acquiring thermotolerance is an active process by which considerable amounts of plant resources are diverted to structural and functional maintenance to escape damages caused by heat stress. Although biochemical and molecular aspects of thermotolerance in plants are relatively well understood, further studies focused on phenotypic flexibility and assimilate partitioning under heat stress and factors modulating crop heat tolerance are imperative. Such studies combined with genetic approaches to identify and map genes (or QTLs) conferring thermotolerance will not only facilitate marker-assisted breeding for heat tolerance but also pave the way for cloning and characterization of underlying genetic factors which could be useful for engineering plants with improved heat tolerance.

Introduction

Heat stress is often defined as the rise in temperature beyond a threshold level for a period of time sufficient to cause irreversible damage to plant growth and development. In general, a transient elevation in temperature, usually 10–15 °C above ambient, is considered heat shock or heat stress. However, heat stress is a complex function of intensity (temperature in degrees), duration, and rate of increase in temperature. The extent to which it occurs in specific climatic zones depends on the probability and period of high temperatures occurring during the day and/or the night. Heat tolerance is generally defined as the ability of the plant to grow and produce economic yield under high temperatures. However, while some researchers believe that night temperatures are major limiting factors others have argued that day and night temperatures do not affect the plant independently and that the diurnal mean temperature is a better predictor of plant response to high temperature with day temperature having a secondary role (Peet and Willits, 1998).

Heat stress due to high ambient temperatures is a serious threat to crop production worldwide (Hall, 2001). Gaseous emissions due to human activities are substantially adding to the existing concentrations of greenhouse gases, particularly CO₂, methane, chlorofluorocarbons and nitrous oxides. Different global circulation models predict that greenhouse gases will gradually increase world's average ambient temperature. According to a report of the Intergovernmental Panel on Climatic Change (IPCC), global mean temperature will rise 0.3 °C per decade (Jones et al., 1999) reaching to approximately 1 and 3 °C above the present value by years 2025 and 2100, respectively, and leading to global warming. Rising temperatures may lead to altered geographical distribution and growing season of agricultural crops by allowing the threshold temperature for the start of the season and crop maturity to reach earlier (Porter, 2005).

At very high temperatures, severe cellular injury and even cell death may occur within minutes, which could be attributed to a catastrophic collapse of cellular organization (Schöffl et al., 1999). At moderately high temperatures, injuries or death may occur only after long-term exposure. Direct injuries due to high temperatures include protein denaturation and aggregation, and increased fluidity of membrane lipids. Indirect or slower heat injuries include inactivation of enzymes in chloroplast and mitochondria, inhibition of protein synthesis, protein degradation and loss of membrane integrity (Howarth, 2005). Heat stress also affects the organization of microtubules by splitting and/or elongation of spindles, formation of microtubule asters in mitotic cells, and elongation of phragmoplast microtubules (Smertenko et al., 1997). These injuries eventually lead to starvation, inhibition of growth, reduced ion flux, production of toxic compounds and reactive oxygen species (ROS) (Schöffl et al., 1999, Howarth, 2005).

Immediately after exposure to high temperatures and perception of signals, changes occur at the molecular level altering the expression of genes and accumulation of transcripts, thereby leading to the synthesis of stress-related proteins as a stress-tolerance strategy (Iba, 2002). Expression of heat shock proteins (HSPs) is known to be an important adaptive strategy in this regard (Feder and Hoffman, 1999). The HSPs, ranging in molecular mass from about 10 to 200 kDa, have chaperone-like functions and are involved in signal transduction during heat stress (Schöffl et al., 1999). The tolerance conferred by HSPs results in improved physiological phenomena such as photosynthesis, assimilate partitioning, water and nutrient use efficiency, and membrane stability (Camejo et al., 2005, Ahn and Zimmerman, 2006, Momcilovic and Ristic, 2007). Such improvements make plant growth and development possible under heat stress. However, not all plant species or genotypes within species have similar capabilities in coping with the heat stress. There exists tremendous variation within and between species, providing opportunities to improve crop heat-stress tolerance through genetic means. Some attempts to develop heat-tolerant genotypes via conventional plant breeding protocols have been successful (Ehlers and Hall, 1998, Camejo et al., 2005). Recently, however, advanced techniques of molecular breeding and genetic engineering have provided additional tools, which could be employed to develop crops with improved heat tolerance and to combat this universal environmental adversary. However, to assure achievement of success in this strategy, concerted efforts of plant physiologist, molecular biologists and crop breeders are imperative.

This review accentuates on plant responses and adaptations to heat stress at the whole plant, cellular and sub-cellular levels, tolerance mechanisms and strategies for genetic improvement of crops with heat-stress tolerance.