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Crop reproductive success is significantly challenged by heatwaves, which are increasing in frequency and severity globally. Heat-induced male sterility is mainly due to aborted pollen development, but it is not clear whether this is through direct or systemic effects. Here, long-term mild heat (LTMH) treatment, mimicking a heatwave, was applied locally to tomato flowers or whole plants and followed up by cytological, transcriptomic, and biochemical analyses. By analyzing pollen viability, LTMH was shown to act directly on the flowers and not via effects on other plant tissue. The meiosis to early microspore stage of pollen development was the most sensitive to LTMH and 3 days of exposure around this period was sufficient to significantly reduce pollen viability at the flower anthesis stage. Extensive cytological analysis showed that abnormalities in pollen development could first be observed after pollen mitosis I, while no deviations in tapetum development were observed. Transcriptomic and biochemical analyses suggested that pollen development suffered from tapetal ER stress and that there was a limited role for oxidative stress. Our results provide the first evidence that heat acts directly on flowers to induce pollen sterility, and that the molecular-physiological responses of developing anthers to the LTMH are different from those to severe heat shock.

Exposure to high temperatures leads to failure in pollen development, which may have significant implications for food security with ongoing climate change. We hypothesized that the stress response-associated hormone salicylic acid (SA) affects pollen tolerance to long-term mild heat (LTMH) (≥14 days exposure to day-/nighttime temperature of 30–34/24–28°C, depending on the genotype), either positively, by inducing acclimation, or negatively, by reducing investment in reproductive development. Here, we investigated these hypotheses assessing the pollen thermotolerance of a 35S:nahG tomato line, which has low SA levels. We found that reducing the SA level resulted in increased pollen viability of plants grown in LTMH and further characterized this line by transcriptome, carbohydrate, and hormone analyses. Low expression of JAZ genes in 35S:nahG and LTMH hypersensitivity of low-jasmonic acid (JA) genotypes together suggest that the increased pollen thermotolerance in the low-SA line involves enhanced JA signal in developing anthers in LTMH. These findings have potential application in the development of more thermotolerant crops.

Sexual reproduction in flowering plants is very sensitive to environmental stresses, particularly to thermal insults which frequently occur when plants grow in field conditions in the warm season. Although abnormalities in both male and female reproductive organs due to high temperatures have been described in several crops, the failure to set fruits has mainly been attributed to the high sensitivity of developing anthers and pollen grains, particularly at certain developmental stages. A global view of the molecular mechanisms involved in the response to high temperatures in the male reproductive organs will be presented in this review. In addition, transcriptome and proteomic data, currently available, will be discussed in the light of physiological and metabolic changes occurring during anther and pollen development. A deep understanding of the molecular mechanisms involved in the stress response to high temperatures in flowers and, particularly, in the male reproductive organs will be a major step towards development of effective breeding strategies for high and stable production in crop plants.

Sexual reproduction is a critical process in the life-cycle of plants and very sensitive to environmental perturbations. To better understand the effect of high temperature on plant reproduction, we cultivated tomato (Solanum lycopersicum) plants in continuous mild heat. Under this condition we observed a simultaneous reduction in pollen viability and appearance of anthers with pistil-like structures, while in a more thermotolerant genotype, both traits were improved. Ectopic expression of two pistil-specific genes, TRANSMITTING TISSUE SPECIFIC and TOMATO AGAMOUS LIKE11, in the anthers confirmed that the anthers had gained partial pistil identity. Concomitantly, expression of the B-class genes TOMATO APETALA3, TOMATO MADS BOX GENE6 (TM6) and LePISTILLATA was reduced in anthers under continuous mild heat. Plants in which TM6 was partially silenced reacted hypersensitively to temperature elevation with regard to the frequency of pistilloid anthers, pollen viability and pollen quantity. Taken together, these results suggest that high-temperature-induced down-regulation of tomato B-class genes contributes to anther deformations and reduced male fertility. Improving our understanding of how temperature perturbs the molecular mechanisms of anther and pollen development will be important in the view of maintaining agricultural output under current climate changes.

High temperature has become a global concern because it seriously affects the growth and reproduction of plants. Exposure of plant cells to high temperatures result in cellular damage and can even lead to cell death. Part of the damage can be ascribed to the action of reactive oxygen species (ROS), which accumulate during abiotic stresses such as heat stress. ROS are toxic and can modify other biomacromolecules including membrane lipids, DNA, and proteins. In order to protect the cells, ROS scavenging is essential. In contrast with their inherent harms, ROS also function as signaling molecules, inducing stress tolerance mechanisms. This review examines the evidence for crosstalk between the classical heat stress response, which consists of heat shock factors (HSFs) and heat shock proteins (HSPs), with the ROS network at multiple levels in the heat response process. Heat stimulates HSF activity directly, but also indirectly via ROS. HSFs in turn stimulate the expression of HSP chaperones and also affect ROS scavenger gene expression. In the short term, HSFs repress expression of superoxide dismutase scavenger genes via induction of miRNA398, while they also activate scavenger gene expression and stabilize scavenger protein activity via HSP induction. We propose that these contrasting effects allow for the boosting of the heat stress response at the very onset of the stress, while preventing subsequent oxidative damage. The described model on HSFs, HSPs, ROS, and ROS scavenger interactions seems applicable to responses to stresses other than heat and may explain the phenomenon of crossacclimation. [ABSTRACT FROM AUTHOR]