Pollen Development at High Temperature: From Acclimation to Collapse1[OPEN]

The seeds and fruits derived from the sexual reproduction of flowering plants constitute the major part of the human diet. Our capacity to generate sufficient crop yield is increasingly compromised by human population expansion, competition for land use, biodiversity loss, and global climate change. Hot days and heat waves are predicted to increase in frequency and intensity in many temperate regions in the coming decades as a consequence of global warming (Pachauri et al., 2014). Exposure to high temperature episodes often coincides with the reproductive phase of the plant life cycle. As pollen development and functioning are among the most heat-sensitive processes that impact upon plant fertility, it is crucial to understand the mechanisms and processes underlying heat-related male sterility in order to maintain food security. Sexual plant reproduction in flowering plants involves two central processes: meiosis, which rearranges the genes and reduces the number of chromosomes; and fertilization, which restores the diploid chromosome number. In between these two, haploid spores develop into multicellular gametophytes, which produce the male or female gametes. Development of the male gametophyte (pollen) has been shown to be sensitive to environmental fluctuations and suboptimal conditions, thereby limiting sexual reproduction (Iwahori, 1965; Schoper et al., 1987; Peet et al., 1998; Dupuis andDumas, 1990; Ahmed et al., 1992; Kim et al., 2001). Pollen is formed inside the anther locules from diploid pollenmother cells that undergomeiosis to give rise to a tetrad of four haploid microspores surrounded by locular fluid. After release from the tetrad, the free microspores enlarge and divide asymmetrically (pollen mitosis I) to form a larger vegetative cell and a smaller generative cell. The generative cell is then engulfed by the vegetative cell and undergoes a second mitosis (pollen mitosis II), either before pollen is released from the anther or during pollen tube growth, to form two sperm cells (McCormick, 2004). During the differentiation of the pollen mother cells, the innermost anther wall layer forms the tapetum (Goldberg et al., 1993). This tissue is metabolically active, especially at early microspore stage, providing the developing microspores with carbohydrates, nutrients, enzymes, and compounds required for the synthesis of the outer pollen wall (exine). Development of the tapetum is tightly coordinated with microspore development and its degeneration begins shortly after microspores are