Acute heat stress during stamen development affects both the germline and sporophytic lineages in Arabidopsis thaliana (L.) Heynh.

Abstract

Flowers, from their initiation in the inflorescence meristem until their opening at anthesis, are particularly sensitive to subtle changes in environmental conditions. Short episodes of either cold or heat stress experienced during stamen development may lead to varying degrees of male sterility and can affect the ploidy of the gametes. In an attempt to understand the developmental origins of these and other phenotypes that are caused by harsh environmental conditions, an acute heat stress was simultaneously applied to all stages of anther development, and its consequences on pollen viability at anthesis and seed set were traced back to heat stress at specific developmental stages. We identified a critical stage during microsporogenesis that is highly sensitive to heat stress. The acute heat stress experienced during these stages completely blocked stamen and pollen development, likely mediated by its effects on both anther wall development and the formation of polyads in the germline. Interestingly, as we investigated heat shocks at earlier developmental stages, a gradual recovery of male fertility was observed, characterized by some abnormalities in locule development and by fusions of maturing pollen grains. Overall, our findings establish a developmental framework for the diverse effects of heat stress on stamen and pollen development, which is relevant to different fields of research. Acute heat stresses are expected to increase in frequency with global warming and might negatively affect plant fitness and crop yields in the short term by affecting male fertility and seed set. Moreover, the formation of polyads and the fusion of pollen grains offer insights into the developmental origins of evolutionary relevant processes, such as polyploidization, which might offer opportunities for environmental adaptations in the long term.