Abstract Thermal environments vary widely across species ranges, establishing the potential for local adaptation of thermal performance optima and tolerance. In the absence of local adaptation, selection should favor mechanisms to meet thermal optima. Floral temperature is a major determinant of reproductive success in angiosperms, yet whether gametic thermal performance shows signatures of local adaptation across temperature gradients, and how variation in gametic thermal performance influences floral evolution, is unknown. We characterized flowering season temperatures for the forb, Argentina anserina, at extremes of a 1000 m elevation gradient and generated thermal performance curves for pollen and ovule performance in populations at each extreme. Thermal optima fell between mean and maximum intrafloral temperatures. However, cooler high-elevation populations had ~4 °C greater pollen thermal optima than warmer low-elevation populations, while tolerance breadths did not differ. We then tested whether plants at elevational extremes differentially warmed the floral microenvironment. High-elevation flowers warmed significantly more than low, bringing intrafloral temperatures nearer the pollen optima. A manipulative experiment demonstrated that stronger warming in high elevation was conferred by floral tissues. Elevational divergence in floral warming may be driven, in part, by selection on flowers to meet different thermal demands of the gametophytes.
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PIF4 negatively modulates cold tolerance in tomato anthers via temperature-dependent regulation of tapetal cell death
Abstract Extreme temperature conditions seriously impair male reproductive development in plants; however, the molecular mechanisms underlying the response of anthers to extreme temperatures remain poorly described. The transcription factor phytochrome-interacting factor4 (PIF4) acts as a hub that integrates multiple signaling pathways to regulate thermosensory growth and architectural adaptation in plants. Here, we report that SlPIF4 in tomato (Solanum lycopersicum) plays a pivotal role in regulating cold tolerance in anthers. CRISPR (clustered regularly interspaced short palindromic repeats)–associated nuclease Cas9-generated SlPIF4 knockout mutants showed enhanced cold tolerance in pollen due to reduced temperature sensitivity of the tapetum, while overexpressing SlPIF4 conferred pollen abortion by delaying tapetal programmed cell death (PCD). SlPIF4 directly interacts with SlDYT1, a direct upstream regulator of SlTDF1, both of which (SlDYT1 and SlTDF1) play important roles in regulating tapetum development and tapetal PCD. Moderately low temperature (MLT) promotes the transcriptional activation of SlTDF1 by the SlPIF4–SlDYT1 complex, resulting in pollen abortion, while knocking out SlPIF4 blocked the MLT-induced activation of SlTDF1. Furthermore, SlPIF4 directly binds to the canonical E-box sequence in the SlDYT1 promoter. Collectively, these findings suggest that SlPIF4 negatively regulates cold tolerance in anthers by directly interacting with the tapetal regulatory module in a temperature-dependent manner. Our results shed light on the molecular mechanisms underlying the adaptation of anthers to low temperatures.
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- Award ID(s):
- 1855585
- PAR ID:
- 10321888
- Date Published:
- Journal Name:
- The Plant Cell
- Volume:
- 33
- Issue:
- 7
- ISSN:
- 1040-4651
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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