skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.
Attention:The NSF Public Access Repository (NSF-PAR) system and access will be unavailable from 7:00 AM ET to 7:30 AM ET on Friday, April 24 due to maintenance. We apologize for the inconvenience.


Title: 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.  more » « less
Award ID(s):
1855585
PAR ID:
10321888
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ;
Date Published:
Journal Name:
The Plant Cell
Volume:
33
Issue:
7
ISSN:
1040-4651
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Friedman, Jannice; Connallon, Tim (Ed.)
    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. 
    more » « less
  2. Due to its tropical origin and adaptation, rice is significantly impacted by cold stress, and consequently sustains large losses in growth and productivity. Currently, rice is the second most consumed cereal in the world and production losses caused by extreme temperature events in the context of "major climatic changes" can have major impacts on the world economy. We report here an analysis of rice genotypes in response to low-temperature stress, studied through physiological gas-exchange parameters, biochemical changes in photosynthetic pigments and antioxidants, and at the level of gene and protein expression, towards an understanding and identification of multiple low-temperature tolerance mechanisms. The first effects of cold stress were observed on photosynthesis among all genotypes. However, the tropical japonica genotypes Secano do Brazil and Cypress had a greater reduction in gas exchange parameters like photosynthesis and water use efficiency in comparison to the temperate japonica Nipponbare and M202 genotypes. The analysis of biochemical profiles showed that despite the impacts of low temperature on tolerant plants, they quickly adjusted to maintain their cellular homeostasis by an accumulation of antioxidants and osmolytes like phenolic compounds and proline. The cold tolerant and sensitive genotypes showed a clear difference in gene expression at the transcript level for OsGH3-2, OsSRO1a, OsZFP245, and OsTPP1, as well as for expression at the protein level for LRR-RLKs, bHLH, GLYI, and LTP1 proteins. This study exemplifies the cold tolerant features of the temperate japonica Nipponbare and M202 genotypes, as observed through the analysis of physiological and biochemical responses and the associated changes in gene and protein expression patterns. The genes and proteins showing differential expression response are notable candidates towards understanding the biological pathways affected in rice and for engineering cold tolerance, to generate cultivars capable of maintaining growth, development, and reproduction under cold stress. We also propose that the mechanisms of action of the genes analyzed are associated with the tolerance response. 
    more » « less
  3. Sopory, SK (Ed.)
    As sessile organisms, plants are constantly exposed to a variety of environmental stresses that have detrimental effects on their growth and development, leading to major crop yield losses worldwide. To cope with adverse conditions plants have developed several adaptive mechanisms. A thorough understanding these mechanisms is critical to generate plants for the future. The heterotrimeric G-protein complex, composed of Gα, Gβ, and Gγ subunits, participates in regulation of multiple cellular signaling pathways and have multifaceted roles in regulating stress responses of plants. The complex has two functional entities, the GTP-bound Gα subunit and the Gβγ dimer, both of which by interacting with additional proteins can activate various signaling networks. The involvement of G-proteins has been shown in plants’ response to drought, salinity, extreme temperatures, heavy metal, ozone, and UV-B radiation. Due to their versatility and the number of processes modulated by them, G-proteins have emerged as key targets for generating stress tolerant crops. In this review, we provide an overview of the current knowledge of the roles of G proteins in abiotic stress tolerance, with examples from model plant Arabidopsis thaliana, where these processes are most widely studied and from additional agriculturally relevant crops, where their potential is realized for human usage. 
    more » « less
  4. Abstract The floral microenvironment impacts gametophyte viability and plant–pollinator interactions. Plants employ mechanisms to modify floral temperature, including thermogenesis, absorption of solar radiation, and evaporative cooling. Whether floral thermoregulation impacts reproductive fitness, and how floral morphological variation mediates thermoregulatory capacity are poorly understood.We measured temperature of the floral microenvironment in the field and tested for thermogenesis in the lab in early spring floweringHexastylis arifolia(Aristolochiaceae). We evaluated whether thermoregulatory capacity was associated with floral morphological variation. Finally, we experimentally determined the thermal optimum and tolerance of pollen to assess whether thermoregulation may ameliorate thermal stress to pollen.Pollen germination was optimal near 21 °C, with a 50% tolerance breadth of ~18 °C. In laboratory conditions, flowers exhibited thermogenesis of 1.5–4.8 °C for short intervals within a conserved timeframe (08:00–09:00 h). In the field, temperature inside the floral tube often deviated from ambient – floral interiors were up to 4 °C above ambient when it was cold, but some fell nearly 10 °C below ambient during peak heat. Flowers with smaller openings were cooler and more thermally stable than those with larger openings during peak heat. Thermoregulation maintained a floral microenvironment within the thermal tolerance breadth of pollen.Results suggest thatH. arifoliaflowers have a stronger capacity to cool than to warm, and that narrower floral openings create a distinct floral microenvironment, enhancing floral cooling effects. While deviation of floral temperature from ambient conditions maintains a suitable environment for pollen and suggests an adaptive role of thermoregulation, we discuss adaptive and nonadaptive mechanisms underlying floral warming and cooling. 
    more » « less
  5. Climate change affects the agricultural sector by modifying precipitation patterns, increasing extreme weather events, and geographically shifting agriculturally viable areas. These climate alterations substantially impact plant resilience to abiotic stress and, consequently, agricultural productivity. A better understanding of plant adaptations to tolerate extreme environmental conditions could pave the way for future advances in agricultural sustainability. One such adaptation is vegetative desiccation tolerance (VDT), which enables some species, known as ‘resurrection plants’, to undergo almost complete drying without losing viability. The current review discusses how incorporating different molecular and biochemical mechanisms underlying VDT into crops might expand the time during which crops can continue growing under limiting water conditions and perhaps broaden the range of survivable negative water potentials that a crop can endure under drought stress. Such possibilities could alleviate the detrimental consequences of low water availability to crops. Understanding how plants survive extreme dehydration has the potential to enlighten new strategies to improve the climate resiliency of crops, thereby positively impacting worldwide food security and sustainability. 
    more » « less