Untargeted metabolomic analysis of tomato pollen development and heat stress response

Paupière, Marine J.; Müller, Florian; Li, Hanjing; Rieu, Ivo; Tikunov, Yury; Visser, R.G.F.; Bovy, Arnaud

doi:10.1007/s00497-017-0301-6

Cited by 80 publications

(79 citation statements)

References 74 publications

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“…Several studies have suggested that flavonols are part of the heat-stress response in vegetative and reproductive tissues. Indeed, transcript abundances and enzyme activities of flavonol biosynthetic genes (39), as well as flavonol pools (39,42), increase during heat stress in tomato leaves and pollen grains. Therefore, we analyzed the effect of acute heat stress on tomato pollen tube growth and ROS levels.…”

Section: Discussionmentioning

confidence: 99%

“…Heat stress increases ROS production, which results in distinct transcriptional responses (38), including increased abundance of transcripts and proteins involved in ROS scavenging (39)(40)(41). Elevated temperature has been shown to increase flavonol biosynthesis in vegetative tissues (39), as well as in developing pollen (42). However, the involvement of flavonols as antioxidants against high-temperature-induced ROS has not been reported.…”

Section: Significancementioning

confidence: 99%

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Flavonols control pollen tube growth and integrity by regulating ROS homeostasis during high-temperature stress

Mühlemann

Younts

Muday

2018

Proc. Natl. Acad. Sci. U.S.A.

245

259

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Plant reproduction requires long-distance growth of a pollen tube to fertilize the female gametophyte. Prior reports suggested that mutations altering synthesis of flavonoids, plant specialized metabolites that include flavonols and anthocyanins, impair pollen development in several species, but the mechanism by which flavonols enhanced fertility was not defined. Here, we used genetic approaches to demonstrate that flavonols enhanced pollen development by reducing the abundance of reactive oxygen species (ROS). We further showed that flavonols reduced high-temperature stress-induced ROS accumulation and inhibition of pollen tube growth. The anthocyanin reduced (are) tomato mutant had reduced flavonol accumulation in pollen grains and tubes. This mutant produced fewer pollen grains and had impaired pollen viability, germination, tube growth, and tube integrity, resulting in reduced seed set. Consistent with flavonols acting as ROS scavengers, are had elevated levels of ROS. The pollen viability, tube growth and integrity defects, and ROS accumulation in are were reversed by genetic complementation. Inhibition of ROS synthesis or scavenging of excess ROS with an exogenous antioxidant treatment also reversed the are phenotypes, indicating that flavonols function by reducing ROS levels. Heat stress resulted in increased ROS in pollen tubes and inhibited tube growth, with more pronounced effects in the are mutant that could be rescued by antioxidant treatment. These results are consistent with increased ROS inhibiting pollen tube growth and with flavonols preventing ROS from reaching damaging levels. These results reveal that flavonol metabolites regulate plant sexual reproduction at both normal and elevated temperatures by maintaining ROS homeostasis.

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Section: Discussionmentioning

confidence: 99%

Section: Significancementioning

confidence: 99%

Flavonols control pollen tube growth and integrity by regulating ROS homeostasis during high-temperature stress

Mühlemann

Younts

Muday

2018

Proc. Natl. Acad. Sci. U.S.A.

245

259

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“…Heat stress affects composition in the primary and secondary metabolites (carbohydrates, lipids, proline, polyamines, glutathione, and flavonoids) [14,28]. A decrease in pollen viability is often associated with an alteration of metabolite contents such as soluble sugars and starch [5,29].…”

Section: Discussionmentioning

confidence: 99%

Identification of Heat-Induced Proteomes in Tomato Microspores Using LCM- Proteomics Analysis

H¹,

Zhu²,

Rangu³

et al. 2018

SCB

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Pollen development is highly susceptible to heat stress (HS) and the production of inviable pollen causes reduction in seed-and fruit-set in plants. This study was carried out to identify HS-induced pollen proteins and the associated biological processes in tomato (Solanum lycopersicum). Tomato 'Micro-Tom' plants were incubated under 32°C//22°C (day/night, 12/12 h) for two weeks for heat treatment, and the non-treated control plants were incubated for the same time period at 25°C /22°C. Flower buds of 5 mm in length were confirmed to contain the heat sensitive uninucleate microspores. Pollen cells were harvested using laser capture microdissection (LCM) and protein was extracted using a one-step method under high pressure and vacuum. Approximately 60,000 LCMharvested microspore cells yielded about 18-20 μg proteins. The tandem mass tags (TMT) proteomics analysis identified a total of 6018 proteins, 4784 proteins were quantified, 37 proteins were identified as HS up-regulated significantly changed proteins (SCPs), and 83 proteins as HS down (dn)-regulated SCPs. Further analysis using the plant MetGenMap system showed that the HS up-regulated SCPs were enriched in the heat acclimation, pollen wall formation, protein folding/refolding gene ontology (GO) biological processes, and the HS dn-regulated SCPs were placed in the carbohydrate catabolism and de-novo protein biosynthesis GO terms. Biological processes such as mitosis, resistance to oxidative stresses, and carbohydrate and lipid metabolic processes contain both the HS up-, and dn-regulated SCPs. These results indicate that the LCM-TMT proteomics workflow is highly efficient in the identification of HS-induced pollen proteomes. These HS induced SCPs will be used for exploring heat tolerance of tomato pollens. The proteomics data are available via ProteomeXchange with identifier PXD010218.

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“…These tolerant types also produced low concentrations of many metabolites, such as chiro-inositol, pinitol, erythritol, and arabitol [157]. Metabolomics analysis was also performed for other important crops, such as tomato, maize, and wheat, to observe the effects of heat stress [158][159][160].…”

Section: Temperature Stress Regulationmentioning

confidence: 99%

Metabolomics: A Way Forward for Crop Improvement

et al. 2019

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Metabolomics is an emerging branch of “omics” and it involves identification and quantification of metabolites and chemical footprints of cellular regulatory processes in different biological species. The metabolome is the total metabolite pool in an organism, which can be measured to characterize genetic or environmental variations. Metabolomics plays a significant role in exploring environment–gene interactions, mutant characterization, phenotyping, identification of biomarkers, and drug discovery. Metabolomics is a promising approach to decipher various metabolic networks that are linked with biotic and abiotic stress tolerance in plants. In this context, metabolomics-assisted breeding enables efficient screening for yield and stress tolerance of crops at the metabolic level. Advanced metabolomics analytical tools, like non-destructive nuclear magnetic resonance spectroscopy (NMR), liquid chromatography mass-spectroscopy (LC-MS), gas chromatography-mass spectrometry (GC-MS), high performance liquid chromatography (HPLC), and direct flow injection (DFI) mass spectrometry, have sped up metabolic profiling. Presently, integrating metabolomics with post-genomics tools has enabled efficient dissection of genetic and phenotypic association in crop plants. This review provides insight into the state-of-the-art plant metabolomics tools for crop improvement. Here, we describe the workflow of plant metabolomics research focusing on the elucidation of biotic and abiotic stress tolerance mechanisms in plants. Furthermore, the potential of metabolomics-assisted breeding for crop improvement and its future applications in speed breeding are also discussed. Mention has also been made of possible bottlenecks and future prospects of plant metabolomics.

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Untargeted metabolomic analysis of tomato pollen development and heat stress response

Cited by 80 publications

References 74 publications

Flavonols control pollen tube growth and integrity by regulating ROS homeostasis during high-temperature stress

Flavonols control pollen tube growth and integrity by regulating ROS homeostasis during high-temperature stress

Identification of Heat-Induced Proteomes in Tomato Microspores Using LCM- Proteomics Analysis

Metabolomics: A Way Forward for Crop Improvement

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