Heat tolerance in plants: An overview

Stressful environments such as salinity, drought, and high temperature (heat) cause alterations in a wide range of physiological, biochemical, and molecular processes in plants. Photosynthesis, the most fundamental and intricate physiological process in all green plants, is also severely affected in all its phases by such stresses. Since the mechanism of photosynthesis involves various components, including photosynthetic pigments and photosystems, the electron transport system, and CO2 reduction pathways, any damage at any level caused by a stress may reduce the overall photosynthetic capacity of a green plant. Details of the stress-induced damage and adverse effects on different types of pigments, photosystems, components of electron transport system, alterations in the activities of enzymes involved in the mechanism of photosynthesis, and changes in various gas exchange characteristics, particularly of agricultural plants, are considered in this review. In addition, we discussed also progress made during the last two decades in producing transgenic lines of different C3 crops with enhanced photosynthetic performance, which was reached by either the overexpression of C3 enzymes or transcription factors or the incorporation of genes encoding C4 enzymes into C3 plants. We also discussed critically a current, worldwide effort to identify signaling components, such as transcription factors and protein kinases, particularly mitogen-activated protein kinases (MAPKs) involved in stress adaptation in agricultural plants.

Photosynthesis under stressful environments: An overview

Complexity of the heat stress response in plants.

Reactive oxygen species (ROS) are known as toxic metabolic products in plants and other aerobic organisms. An elaborate and highly redundant plant ROS network, composed of antioxidant enzymes, antioxidants and ROS-producing enzymes, is responsible for maintaining ROS levels under tight control. This allows ROS to serve as signaling molecules that coordinate an astonishing range of diverse plant processes. The specificity of the biological response to ROS depends on the chemical identity of ROS, intensity of the signal, sites of production, plant developmental stage, previous stresses encountered and interactions with other signaling molecules such as nitric oxide, lipid messengers and plant hormones. Although many components of the ROS signaling network have recently been identified, the challenge remains to understand how ROS-derived signals are integrated to eventually regulate such biological processes as plant growth, development, stress adaptation and programmed cell death.

Reactive oxygen species as signals that modulate plant stress responses and programmed cell death.

https://eprints.cs.univie.ac.at/3231/1/0-S1874939911001787-main.pdf

The plant heat stress transcription factor (Hsf) family: structure, function and evolution.

The expression of heat shock proteins (Hsps) induced by nonlethal heat treatment confers acquired thermotolerance (AT) to organisms against subsequent challenges of otherwise lethal temperature. After the stress signal is removed, AT gradually decays, with decreased Hsps during recovery. AT of sufficient duration is critical for sessile organisms such as plants to survive repeated heat stress in their environment, but little is known regarding its regulation. To identify potential regulatory components, we took a reverse genetics approach by screening for Arabidopsis (Arabidopsis thaliana) T-DNA insertion mutants that show decreased thermotolerance after a long recovery (2 d) under nonstress conditions following an acclimation heat treatment. Among the tested mutants corresponding to 48 heat-induced genes, only the heat shock transcription factor HsfA2 knockout mutant showed an obvious phenotype. Following pretreatment at 37°C, the mutant line was more sensitive to severe heat stress than the wild type after long but not short recovery periods, and this could be complemented by the introduction of a wild-type copy of the HsfA2 gene. Quantitative hypocotyl elongation assay also revealed that AT decayed faster in the absence of HsfA2. Significant reduction in the transcript levels of several highly heat-inducible genes was observed in HsfA2 knockout plants after 4 h recovery or 2 h prolonged heat stress. Immunoblot analysis showed that Hsa32 and class I small Hsp were less abundant in the mutant than in the wild type after long recovery. Our results suggest that HsfA2 as a heat-inducible transactivator sustains the expression of Hsp genes and extends the duration of AT in Arabidopsis.

/pdf/a-heat-inducible-transcription-factor-hsfa2-is-required-for-ifad2ckn48.pdf

A Heat-Inducible Transcription Factor, HsfA2, Is Required for Extension of Acquired Thermotolerance in Arabidopsis

The expression of heat shock proteins (Hsps) induced by nonlethal heat treatment confers acquired thermotolerance (AT) toorganisms against subsequent challenges of otherwise lethal temperature. After the stress signal is removed, AT graduallydecays, with decreased Hsps during recovery. ATof sufﬁcient duration is critical for sessile organisms such as plants to surviverepeated heat stress in their environment, but little is known regarding its regulation. To identify potential regulatorycomponents, we took a reverse genetics approach by screening for Arabidopsis (Arabidopsis thaliana) T-DNA insertion mutantsthat show decreased thermotolerance after a long recovery (2 d) under nonstress conditions following an acclimation heattreatment. Among the tested mutants corresponding to 48 heat-induced genes, only the heat shock transcription factor HsfA2knockout mutant showed an obvious phenotype. Following pretreatment at 37 C, the mutant line was more sensitive to severeheat stress than the wild type after long but not short recovery periods, and this could be complemented by the introduction ofa wild-type copy of the HsfA2 gene. Quantitative hypocotyl elongation assay also revealed that AT decayed faster in theabsence of HsfA2. Signiﬁcant reduction in the transcript levels of several highly heat-inducible genes was observed in HsfA2knockout plants after 4 h recovery or 2 h prolonged heat stress. Immunoblot analysis showed that Hsa32 and class I small Hspwere less abundant in the mutant than in the wild type after long recovery. Our results suggest that HsfA2 as a heat-inducibletransactivator sustains the expression of Hsp genes and extends the duration of AT in Arabidopsis.

A Heat-Inducible Transcription Factor, HsfA2, Is Required for Extension of Acquired Thermotolerance

Plants and animals share similar mechanisms in the heat shock (HS) response, such as synthesis of the conserved HS proteins (Hsps). However, because plants are confined to a growing environment, in general they require unique features to cope with heat stress. Here, we report on the analysis of the function of a novel Hsp, heat-stress-associated 32-kD protein (Hsa32), which is highly conserved in land plants but absent in most other organisms. The gene responds to HS at the transcriptional level in moss (Physcomitrella patens), Arabidopsis (Arabidopsis thaliana), and rice (Oryza sativa). Like other Hsps, Hsa32 protein accumulates greatly in Arabidopsis seedlings after HS treatment. Disruption of Hsa32 by T-DNA insertion does not affect growth and development under normal conditions. However, the acquired thermotolerance in the knockout line was compromised following a long recovery period (>24 h) after acclimation HS treatment, when a severe HS challenge killed the mutant but not the wild-type plants, but no significant difference was observed if they were challenged within a short recovery period. Quantitative hypocotyl elongation assay also revealed that thermotolerance decayed faster in the absence of Hsa32 after a long recovery. Similar results were obtained in Arabidopsis transgenic plants with Hsa32 expression suppressed by RNA interference. Microarray analysis of the knockout mutant indicates that only the expression of Hsa32 was significantly altered in HS response. Taken together, our results suggest that Hsa32 is required not for induction but rather maintenance of acquired thermotolerance, a feature that could be important to plants.

Arabidopsis Hsa32, a Novel Heat Shock Protein, Is Essential for Acquired Thermotolerance during Long Recovery after Acclimation

Isolation and characterization of tomato Hsa32 encoding a novel heat-shock protein

Hsa32 is a novel heat-shock protein (Hsp) mainly found in land plants. Recently, it was shown to be essential for acquired thermotolerance following a long recovery after acclimation heat-shock (HS) treatment. Without Hsa32, Arabidopsis mutant plants become more sensitive to severe HS than wildtype plants due to faster decay of a previously acquired protection. Sequence homology showed Hsa32 to be a phosphosulfolactate synthase-related protein, and it was proposed to be involved in the biosynthesis of sulfoquinovosyl diacylglycerol (SQDG), one of the major sulfur-containing glycolipids in the chloroplast thylakoid membrane. Currently, Sqd1 and Sqd2 are known to catalyze the consecutive reactions in the biosynthetic pathway of the sulfolipid. In this study, we examine Hsa32's possible involvement in an alternative pathway that bypasses Sqd1. Our analysis of the wild type and Hsa32 T-DNA knockout mutant plants revealed no significant differences in SQDG accumulation. In addition, the Arabidopsis mutant with a disrupted Sqd1 gene did not synthesize SQDG, which discounts the existence of an alternative pathway. The Sqd1 and Sqd2 knockout mutants, both lacking SQDG, did not show the same defect in acquired thermotolerance as did the Hsa32 null mutant, which suggests that the sulfolipid level is not related to the HS-sensitive phenotype. Our data suggest that Hsa32 is not involved in SQDG biosynthesis.

/pdf/hsa32-a-phosphosulfolactate-synthase-related-heat-shock-193pulen3o.pdf

Nai-yu Liu

Papers

A Heat-Inducible Transcription Factor, HsfA2, Is Required for Extension of Acquired Thermotolerance in Arabidopsis

A Heat-Inducible Transcription Factor, HsfA2, Is Required for Extension of Acquired Thermotolerance

Arabidopsis Hsa32, a Novel Heat Shock Protein, Is Essential for Acquired Thermotolerance during Long Recovery after Acclimation

Isolation and characterization of tomato Hsa32 encoding a novel heat-shock protein

Hsa32, a Phosphosulfolactate Synthase-related heat-shock Protein, is Not Involved in Sulfolipid Biosynthesis in Arabidopsis