Maize cytosolic invertase INVAN6 ensures faithful meiotic progression under heat stress

Faithful meiotic progression ensures the generation of viable gametes. Studies suggested the male meiosis of plants is sensitive to ambient temperature, but the underlying molecular mechanisms remain elusive. Here, we characterized a maize (Zea mays ssp. mays L.) dominant male sterile mutant Mei025, in which the meiotic process of pollen mother cells (PMCs) was arrested after pachytene. An Asp-to-Asn replacement at position 276 of INVERTASE ALKALINE NEUTRAL 6 (INVAN6), a cytosolic invertase (CIN) that predominantly exists in PMCs and specifically hydrolyses sucrose, was revealed to cause meiotic defects in Mei025. INVAN6 interacts with itself as well as with four other CINs and seven 14-3-3 proteins. Although INVAN6(Mei025), the variant of INVAN6 found in Mei025, lacks hydrolytic activity entirely, its presence is deleterious to male meiosis, possibly in a dominant negative repression manner through interacting with its partner proteins. Notably, heat stress aggravated meiotic defects in invan6 null mutant. Further transcriptome data suggest INVAN6 has a fundamental role for sugar homeostasis and stress tolerance of male meiocytes. In summary, this work uncovered the function of maize CIN in male meiosis and revealed the role of CIN-mediated sugar metabolism and signalling in meiotic progression under heat stress.