An official website of the United States government
Elevated temperatures impair pollen performance and reproductive success, resulting in lower crop yields. The tomato (Solanum lycopersicum) anthocyanin reduced (are) mutant harbors a mutation in FLAVANONE 3-HYDROXYLASE (F3H), resulting in impaired flavonol antioxidant biosynthesis. The are mutant has reduced pollen performance and seed set relative to the VF36 parental line, phenotypes that are accentuated at elevated temperatures. Transformation of are with the wild-type F3H gene, or chemical complementation with flavonols, prevented temperature-dependent reactive oxygen species (ROS) accumulation in pollen and restored the reduced viability, germination, and tube elongation of are to VF36 levels. Overexpression of F3H in VF36 prevented temperature-driven ROS increases and impaired pollen performance, revealing that flavonol biosynthesis promotes thermotolerance. Although stigmas of are had reduced flavonol and elevated ROS levels, the growth of are pollen tubes was similarly impaired in both are and VF36 pistils. RNA-seq was performed at optimal and stress temperatures in are, VF36, and the F3H overexpression line at multiple timepoints across pollen tube elongation. The number of differentially expressed genes increased over time under elevated temperatures in all genotypes, with the greatest number in are. These findings suggest potential agricultural interventions to combat the negative effects of heat-induced ROS in pollen that lead to reproductive failure.
more »
« less
Enhanced Reproductive Thermotolerance of the Tomato high pigment 2 Mutant Is Associated With Increased Accumulation of Flavonols in Pollen
Climate change has created an environment where heat stress conditions are becoming more frequent as temperatures continue to raise in crop production areas around the world. This situation leads to decreased crop production due to plant sensitivity to heat stress. Reproductive success is critically dependent on plants’ ability to produce functional pollen grains, which are the most thermo-sensitive tissue. Flavonols are plant secondary metabolites known for their potent antioxidative activity, essential for male fertility in several species including tomato, and implicated in heat stress tolerance. Since flavonols are highly abundant in fruits of the tomato high pigment 2 ( hp2 ) mutant, we tested the level of flavonols in pollen of this mutant, under the hypothesis that increased accumulation of flavonols would render pollen more tolerant to heat stress. Indeed, pollen from two alleles of the hp2 mutant was found to have flavonols levels increased by 18 and 280% compared with wild-type (WT) under moderate chronic heat stress (MCHS) conditions. This mutant produced on average 7.8-fold higher levels of viable pollen and displayed better germination competence under heat stress conditions. The percentage of fully seeded fruits and the number of seeds per fruit were maintained in the mutant under heat stress conditions while decreased in wild-type plants. Our results strongly suggest that increased concentrations of pollen flavonols enhance pollen thermotolerance and reproductive success under heat stress conditions. Thus, the high flavonols trait may help frame the model for improving crop resilience to heat stress.
more »
« less
- Award ID(s):
- 1656774
- PAR ID:
- 10390808
- Date Published:
- Journal Name:
- Frontiers in Plant Science
- Volume:
- 12
- ISSN:
- 1664-462X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Rising temperature extremes during critical reproductive periods threaten the yield of major grain and fruit crops. Flowering plant reproduction depends on the ability of pollen grains to generate a pollen tube, which elongates through the pistil to deliver sperm cells to female gametes for double fertilization. We used tomato as amodel fruit croptodeterminehowhigh temperature affects the pollen tube growthphase, takingadvantage of cultivars noted for fruit production in exceptionally hot growing seasons. We found that exposure to high temperature solely during the pollen tube growth phase limits fruit biomass and seed set more significantly in thermosensitive cultivars than in thermotolerant cultivars. Importantly, we found that pollen tubes from the thermotolerantTamaulipas cultivar have enhanced growth in vivo and in vitro under high temperature. Analysis of the pollen tube transcriptome’s response to high temperature allowed us to define two responsemodes (enhanced induction of stress responses and higher basal levels of growth pathways repressed by heat stress) associated with reproductive thermotolerance. Importantly, we define key components of the pollen tube stress response, identifyingenhancedreactive oxygenspecies (ROS)homeostasis andpollen tubecallose synthesis and deposition as important components of reproductive thermotolerance in Tamaulipas. Our work identifies the pollen tube growth phase as a viable target to enhance reproductive thermotolerance and delineates key pathways that are altered in crop varieties capable of fruiting under high-temperature conditions.more » « less
-
In a search for efficient fungal endophytes that can promote crop production and/or increase crop tolerance to abiotic stress, we isolated and tested various species harbored by wild plants. Sixty-seven endophytic fungal isolates were obtained from drought stressed, poor soil habitats, and inland high salt areas. We extensively tested the roles of Ampelomyces sp. and Penicillium sp. isolates in improving tomato growth and yield. Under greenhouse and field trails, Ampelomyces sp. and Penicillium sp. endophytes proved effective in conferring positive benefits to tomatoes placed under stress as well as under normal growing conditions. Ampelomyces sp. conferred tolerance to tomatoes placed under drought stress in addition to enhancing overall plant growth and fruit yield in comparison to non-symbiotic plants under drought stress. Penicillium sp. conferred tolerance to tomatoes placed under 300 mM salinity stress in addition to enhancing root biomass in comparison to non-symbiotic plants. Both endophytes proved efficient in enhancing plant growth, stress tolerance, recovery, and fruit yield under optimal experimental conditions in comparison to non-symbiotic plants. Field testing of tomato yield showed increased yield of symbiotic tomatoes compared to non-symbiotic ones. This data suggests that both Ampelomyces sp. and Penicillium sp. share a promising potential for improving future agricultural production, particularly with the projected changes in climate in the future.more » « less
-
Summary Increasing populations and temperatures are expected to escalate food demands beyond production capacities, and the development of maize lines with better performance under heat stress is desirable. Here, we report that constitutive ectopic expression of a heterologous glutaredoxin S17 fromArabidopsis thaliana(AtGRXS17) can provide thermotolerance in maize through enhanced chaperone activity and modulation of heat stress‐associated gene expression. The thermotolerant maize lines had increased protection against protein damage and yielded a sixfold increase in grain production in comparison to the non‐transgenic counterparts under heat stress field conditions. The maize lines also displayed thermotolerance in the reproductive stages, resulting in improved pollen germination and the higher fidelity of fertilized ovules under heat stress conditions. Our results present a robust and simple strategy for meeting rising yield demands in maize and, possibly, other crop species in a warming global environment.more » « less
-
Differential transpiration is a newly discovered acclimation strategy of annual plants that mitigates the negative impacts of combined water deficit (WD) and heat stress (HS) on plant reproduction. Under conditions of WD + HS, transpiration of vegetative tissues is suppressed in plants such as soybean and tomato, while transpiration of reproductive tissues is not (termed ‘Differential Transpiration’; DT). This newly identified acclimation process enables the cooling of reproductive organs under conditions of WD + HS, limiting HS‐induced damage to plant reproduction. However, the thresholds at which DT remains active and effectively cools reproductive tissues, as well as the developmental stages at which it is activated in soybean, remain unknown. Here, we report that DT occurs at most nodes (leaf developmental stages) of soybean plants subjected to WD + HS, and that it can function under extreme conditions of WD + HS (i.e.,18% of field water capacity and 42°C combined). Our findings reveal that DT is an effective acclimation strategy that protects reproductive processes from extreme conditions of WD + HS at almost all developmental stages. In addition, our findings suggest that, under field conditions, DT could also be active in plants subjected to low or mild levels of WD during a heat wave.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3389/fpls.2021.672368
