OsCNGC13 promotes seed-setting rate by facilitating pollen tube growth in stylar tissues

Abstract

Seed-setting rate is a critical determinant of grain yield in rice (Oryza sativa L.). Rapid and healthy pollen tube growth in the style is required for high seed-setting rate. The molecular mechanisms governing this process remain largely unknown. In this study, we isolate a dominant low seed-setting rate rice mutant, sss1-D. Cellular examination results show that pollen tube growth is blocked in about half of the mutant styles. Molecular cloning and functional assays reveals that SSS1-D encodes OsCNGC13, a member of the cyclic nucleotide-gated channel family. OsCNGC13 is preferentially expressed in the pistils and its expression is dramatically reduced in the heterozygous plant, suggesting a haploinsufficiency nature for the dominant mutant phenotype. We show that OsCNGC13 is permeable to Ca2+. Consistent with this, accumulation of cytoplasmic calcium concentration ([Ca2+]cyt) is defective in the sss1-D mutant style after pollination. Further, the sss1-D mutant has altered extracellular matrix (ECM) components and delayed cell death in the style transmission tract (STT). Based on these results, we propose that OsCNGC13 acts as a novel maternal sporophytic factor required for stylar [Ca2+]cyt accumulation, ECM components modification and STT cell death, thus facilitating the penetration of pollen tube in the style for successful double fertilization and seed-setting in rice.

ROS in the Male–Female Interactions During Pollination: Function and Regulation

“…GRI promotes the superoxide production that triggers cell death (Wrzaczek et al, 2015). Thus, STIG1-promoted pollen tube growth in the pistil tissues might function via mediating ROS-induced PCD of the transmitting tract, as in the rice style (Xu et al, 2017). Rice OsCNGC13, a pistil-preferentially expressed CNGC member, plays roles in Ca 2+ signal-inducing pistil PCD, which facilitates the penetration of the pollen tube in the pistil (Xu et al, 2017).…”

“…Thus, STIG1-promoted pollen tube growth in the pistil tissues might function via mediating ROS-induced PCD of the transmitting tract, as in the rice style (Xu et al, 2017). Rice OsCNGC13, a pistil-preferentially expressed CNGC member, plays roles in Ca 2+ signal-inducing pistil PCD, which facilitates the penetration of the pollen tube in the pistil (Xu et al, 2017). Considering that pollination is an inducer for the PCD of transmitting tissue (Wang et al, 1996;Xu et al, 2017), it is tempting to study whether the apoplastic ROS of the pollen tube growing in transmitting tissue could diffuse into the pistil tissue to trigger the OsCNGC13 activity and pistil PCD in rice ( Figure 1B).…”

CNGCs break through—A rice cyclic nucleotide-gated channel paves the way for pollen tube growth

“…After penetrating the septum, the pollen tube grows through the funiculus and then enters the ovule though the micropyle to deliver the two nonflagellate sperm cells to the two female gametes, leading to double fertilization, a prerequisite to seed formation [ 1 ]. The 2017 study by Xu et al [ 2 ] reveals, for the first time, the importance of a Ca 2+ signal generated by rice cyclic nucleotide-gated channel 13 ( OsCNGC13 ) in the pistil to induce programmed cell death (PCD), which facilitates proper pollen tube growth. Furthermore, they showed this step significantly affects the yield of rice grains.…”

“… The Ca 2+ gradient in pollen tubes is created by members of the CNGC and GLR families (left). Xu et al [ 2 ] reveal a role of OsCNGC13 in the TT of the rice style, where a CNGC-mediated Ca 2+ signal is required to induce cell death, which is necessary for the pollen tube to grow through the TT to reach the ovary (right). A role for CNGCs in PCD formation had been previously shown for AtCNGC11/12 [ 21 ].…”

A Cyclic Nucleotide-Gated Channel, HvCNGC2-3, Is Activated by the Co-Presence of Na+ and K+ and Permeable to Na+ and K+ Non-Selectively

“…The loss-of-function mutation in AtCNGC16 reduced growth and viability of pollen, as well as seed yields [ 27 ]. The rice OsCNGC13 is involved in fertility through function in the pistil [ 28 ]. The Arabidopsis mutant, defense , no death1 ( dnd1 ), was isolated based on the failure of hypersensitive response to avirulent pathogens.…”