Auxins reverse plant male sterility caused by high temperatures

Abstract

With global warming, plant high temperature injury is becoming an increasingly serious problem. In wheat, barley, and various other commercially important crops, the early phase of anther development is especially susceptible to high temperatures. Activation of auxin biosynthesis with increased temperatures has been reported in certain plant tissues. In contrast, we here found that under high temperature conditions, endogenous auxin levels specifically decreased in the developing anthers of barley and Arabidopsis . In addition, expression of the YUCCA auxin biosynthesis genes was repressed by increasing temperatures. Application of auxin completely reversed male sterility in both plant species. These findings suggest that tissue-specific auxin reduction is the primary cause of high temperature injury, which leads to the abortion of pollen development. Thus, the application of auxin may help sustain steady yields of crops despite future climate change.

Genome-Wide Association Mapping of Fertility Reduction upon Heat Stress Reveals Developmental Stage-Specific QTLs in Arabidopsis thaliana

“…Reduction in anther elongation was observed upon heat stress as a result of decreased auxin levels in the developing anthers. Reduced anther elongation upon heat stress has also been found in other species, such as barley (Sakata et al, 2010). The observations of Kim et al (2001) and Warner and Erwin (2005) are in line with our observation that natural variation exists both in terms of duration of the sensitivity window and the degree of reduction in seed set within the sensitivity window.…”

“…These studies showed that heat stress inhibits anther dehiscence, thereby reducing the release of pollen. Heat stress also leads to shortening of the anthers, due to a reduced amount of auxin (Sakata et al, 2010), which results in a mismatch between the ripening of the stigma and anthers, preventing self-fertilization in bisexual monoecious plants. Moreover, viability of pollen is reduced by disruption of male meiosis upon heat stress (Endo et al, 2009).…”

Sensitivity of flowering plant gametophytes to temperature fluctuations

“…A complete understanding of temperature stress on pollen development must await further understanding of carbohydrate turnover during this phase. Interestingly, in a recent study in barley and Arabidopsis, high temperature stress reduced endogenous synthesis of auxin in developing anthers, an effect that was suggested to be related to pollen sterility since exogenously applied auxin restored fertility (Sakata et al, 2010).…”

“…No specific data on seed set but pollen sterility indirectly would reduce seed set in this species Some heat stress/duration combination hampered stamen development (microsporogenesis, filament elongation and pollen maturation) Endogenous auxin synthesis seems to be hampered in anther wall and microspores and could explain sterility as exogenous auxin restored sterility Sakata et al, 2010 Primula sp 6ºC, 15ºC, and 26ºC, 15h/day. Seven populations of five species subjected to 3 different temperatures during 4 days after pollination and then returned to 15ºC.…”

“…Although they were first detected in reproductive tissues two decades ago (Vierling, 1991), their synthesis and function in these tissues are still controversial (Crone et al, 2001;Volkov et al, 2005), and the extent to which they mediate heat stress tolerance in reproductive organs needs to be clarified. Even in the widely characterized vegetative growth, HSPs are not the only players in plant thermotolerance, but additional multiple signaling pathways implicating other components, such as ethylene, abscisic acid, reactive oxygen species and auxin are playing an important role (Kotak et al, 2007;Sakata et al, 2010). A recent expression profiling analysis of maturing tomato microspores subjected to a short heat shock treatment reveals an up-regulation not only of genes implicated in similar pathways, but also of some pollen specific genes that might represent pollen-specific response mechanisms (Frank et al, 2009).…”