HsfA2 Controls the Activity of Developmentally and Stress-Regulated Heat Stress Protection Mechanisms in Tomato Male Reproductive Tissues

Fragkostefanakis, Sotirios; Mesihovic, Anida; Simm, Stefan; Paupière, Marine J.; Hu, Yangjie; Paul, Puneet; Mishra, Sudhish; Tschiersch, Bettina; Theres, Klaus; Bovy, Arnaud; Schleiff, Enrico; Scharf, Klaus Dieter

doi:10.1104/pp.15.01913

Cited by 170 publications

(179 citation statements)

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“…This approach avoids the potential complication of misexpression of the transgene in tissues or cells that otherwise do not express the corresponding endogenous gene, a problem often resulting in pleiotropic effects (e.g. Jin et al, 2009;Fragkostefanakis et al, 2016). We found that tomato fruit set was sustained under LMHS in the CWIN-elevated tomato but dramatically reduced in wild-type plants (Fig.…”

Section: Discussionmentioning

confidence: 64%

“…The other two Hsf proteins, HsfA2 and HsfB1, have also been revealed to play positive roles in heat tolerance of tomato through forming a complex with HsfA1 (Chan-Schaminet et al, 2009;Giorno et al, 2010;Hahn et al, 2011). A recent study showed HsfA2 acts as a coactivator of HsfA1 to control the transcription of heat response genes, including some Hsps, thereby conferring pollen thermotolerance (Fragkostefanakis et al, 2016). Synergistically, constitutive overexpression of Hsp17.7 in carrot (Malik et al, 1999) or Hsp101 in Arabidopsis (Arabidopsis thaliana; Queitsch et al, 2000) increased its heat tolerance.…”

Section: Elevated Cwin Activity Enhances Tomato Fruit Set Under Lmhsmentioning

confidence: 99%

“…Indeed, 2014 and 2015 were the warmest years since records began in 1880 (National Climatic Data Center 2015). In comparison to vegetable growth, plant reproductive development including floral development and fruit and seed set is particularly vulnerable to abiotic stresses (Ruan, 2014;Fragkostefanakis et al, 2016). For example, heat stress can cause 80% floral abortion in tomato (Ruan et al, 2010) and seed or grain abortion of up to 88% in rapeseed (Brassica napus; Young et al, 2004) and maize (Dupuis and Dumas, 1990).…”

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confidence: 99%

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Cell Wall Invertase Promotes Fruit Set under Heat Stress by Suppressing ROS-Independent Cell Death

2016

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Reduced cell wall invertase (CWIN) activity has been shown to be associated with poor seed and fruit set under abiotic stress. Here, we examined whether genetically increasing native CWIN activity would sustain fruit set under long-term moderate heat stress (LMHS), an important factor limiting crop production, by using transgenic tomato (Solanum lycopersicum) with its CWIN inhibitor gene silenced and focusing on ovaries and fruits at 2 d before and after pollination, respectively. We found that the increase of CWIN activity suppressed LMHS-induced programmed cell death in fruits. Surprisingly, measurement of the contents of H 2 O 2 and malondialdehyde and the activities of a cohort of antioxidant enzymes revealed that the CWINmediated inhibition on programmed cell death is exerted in a reactive oxygen species-independent manner. Elevation of CWIN activity sustained Suc import into fruits and increased activities of hexokinase and fructokinase in the ovaries in response to LMHS. Compared to the wild type, the CWIN-elevated transgenic plants exhibited higher transcript levels of heat shock protein genes Hsp90 and Hsp100 in ovaries and HspII17.6 in fruits under LMHS, which corresponded to a lower transcript level of a negative auxin responsive factor IAA9 but a higher expression of the auxin biosynthesis gene ToFZY6 in fruits at 2 d after pollination. Collectively, the data indicate that CWIN enhances fruit set under LMHS through suppression of programmed cell death in a reactive oxygen species-independent manner that could involve enhanced Suc import and catabolism, HSP expression, and auxin response and biosynthesis.

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Section: Discussionmentioning

confidence: 64%

Section: Elevated Cwin Activity Enhances Tomato Fruit Set Under Lmhsmentioning

confidence: 99%

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confidence: 99%

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Cell Wall Invertase Promotes Fruit Set under Heat Stress by Suppressing ROS-Independent Cell Death

2016

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“…In tomato for instance, both a short heat shock and a long-term mildly elevated growth temperature can lead to a significant reduction of pollen numbers and germination potential (Firon et al 2006;Dane et al 1991;Fragkostefanakis et al 2016). To be able to study the effect of heat treatment on pollen metabolome, we applied a heat treatment that did not affect the viability of resulting mature pollen.…”

Section: Impact Of Heat Stressmentioning

confidence: 99%

“…This suggests that other processes than anther contamination may also affect the metabolic composition of obtained pollen using these two isolation procedures. Recently, Fragkostefanakis et al 2016 mentioned that the collection of pollen from anthers can be sorted in two categories: the "released pollen", that is easily released by simple vortexing of the anthers in a solution, and the "unreleased pollen", which represents the pollen grains that remained on the anther wall after vortexing and need mechanical disruption (squeezing) for its release. This distinction makes us speculate that the two releasing methods applied in our study, VSL and AL, may lead to isolation of different pollen types, analogous to the released and unreleased pollen fractions mentioned by Fragkostefanakis et al 2016.…”

Section: The Isolation Of Pollen By Anther Squeezing Causes Metabolicmentioning

confidence: 99%

Identification of metabolites involved in heat stress response in different tomato genotypes

Paupière¹

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Propositions1. Since tomato pollen is sensitive to temperature variations, results from climate chamber experiments with controlled temperature cannot be extrapolated to pollen thermotolerance in commercial tomato production.(this thesis)2. The pollen isolation protocol is a critical determinant for the success of pollen metabolomics studies.(this thesis)3. The choice of the p-value has an undesirably strong influence on a study's conclusions.4. Nutrition should be considered as the first medicine. MeatlessMonday is an effective policy to reduce global warming.6. The health of science rests on scientist's honesty. If Dutch were not Dutch but French, most of them would not speak EnglishPropositions belonging to the thesis, entitled Contents ___________________________________________________________________________ Chapter 1General introduction 1 Chapter 2The metabolic basis of pollen thermo-tolerance: Perspectives for breeding 13 Chapter 3The effect of isolation methods of tomato pollen on the results of metabolic profiling 39 Chapter 4Untargeted metabolomic analysis of tomato pollen development and heat stress response 63 Chapter 5Screening for pollen tolerance to high temperatures in tomato 83 Chapter 6Metabolites associated with thermo-tolerance of tomato pollen 95 Chapter 7General discussion 133 References Climate changeClimate is unequivocally changing. In 2014, IPCC released the fifth assessment report on climate change and stated that "the atmosphere and ocean have warmed, the amounts of snow and ice have diminished and sea level has risen" (IPCC 2014). The main cause for this global warming is extremely likely to be due to anthropogenic activities that are widely acknowledged by climate specialists (Cook et al. 2013). Heat waves and extreme temperatures are expected to be more frequent and to last longer (Meehl and Tebaldi 2004). This climate change is expected to affect the world of today in many ways, including the extinction of species that cannot escape their environment and a decrease in food productivity. For instance, the well documented heat wave of 2003 in Europe led to a yield loss of 25% and 21% for maize and wheat in France, respectively, with an overall economic loss in the European Union estimated at 13 billion euros (IPCC 2007). The direct effect on the human population is not to be underestimated, especially if one takes into account that the world population is predicted to rise from 7.3 billion up to 11 billion by the middle of the 21 st century, thus alarming the decision-makers (Porter and Semenov 2005). From the reduction of greenhouse gas emission with the Kyoto protocol (Oberthur and Hermann 1999) to the recent COP21 agreement to limit the temperature increase of 2˚C (Iyer et al. 2015), policymakers mull over mitigation options. A synergy of policies and adaptation strategies may enhance the efficacy to respond to climate change and limit the consequences on living organisms and ecosystems. The adaption of crops is nested in the identification of genotypes tolerant to temperature...

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Exploring In‐built Defense Mechanisms in Plants under Heat Stress

Surabhi

Seth

2020

Heat Stress Tolerance in Plants

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HsfA2 Controls the Activity of Developmentally and Stress-Regulated Heat Stress Protection Mechanisms in Tomato Male Reproductive Tissues

Cited by 170 publications

References 63 publications

Cell Wall Invertase Promotes Fruit Set under Heat Stress by Suppressing ROS-Independent Cell Death

Cell Wall Invertase Promotes Fruit Set under Heat Stress by Suppressing ROS-Independent Cell Death

Identification of metabolites involved in heat stress response in different tomato genotypes

Exploring In‐built Defense Mechanisms in Plants under Heat Stress

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