Maize cytosolic invertase INVAN6 ensures faithful meiotic progression under heat stress

Abstract

Summary 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 INVAN6Mei025, 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.

The ZmHSF20–ZmHSF4–ZmCesA2 module regulates heat stress tolerance in maize

“…For example, ZmbZIP60 improves the heat tolerance of maize seedlings by increasing the expression of the gene heat up-regulated ( Hug1 ), which influences the stability of proteins in the ER (Li et al, 2020; Xie et al, 2022). Overexpression of ZmHsp101 in maize anthers results in robust microspores under HS (Li et al, 2022); similarly, loss of invertase alkaline neutral 6 (ZmInvan6) function affects the progression of maize meiosis at high temperature and lowers pollen fertility, thus influencing yield (Huang et al, 2022). The transcription factor Necrotic upper tips1 (nut1) participates in heat and drought stress responses by directly influencing cellulose biosynthesis and apoptosis during protoxylem development in maize flowering (Dong et al, 2020).…”

Exploring the role of GhN/AINV23: implications for plant growth, development, and drought tolerance

“…Inhibition of the expression of NtNINV10 decreased the glucose and fructose in tobacco leaves [ 20 ]. INVAN6 plays a key role in the regulation of male meiosis in maize [ 21 ]. The high expression of TaCWI50 and TaVI27 may increase wheat thousand grain weight [ 22 ].…”

Garlic (Allium sativum L.) Invertase Genes: Genome-Wide Identification and Expression in Response to Abiotic Stresses and Phytohormones

“…[14]; thus, in S. tuberosum tubers, VINVs are shown to be responsible for cold-inducing sweetening (negative agricultural trait) [15]. Cytosolic invertases are known to affect sugar homeostasis and stress tolerance of male meiocytes in Z. mays [19] and vegetative growth, flowering, fruit set, and yield in Solanum lycopersicum [20].…”