OsCER1 regulates humidity-sensitive genic male sterility through very-long-chain (VLC) alkane metabolism of tryphine in rice

Abstract

Humidity-sensitive genic male sterility (HGMS) is a novel type of environment-sensitive male sterility (EGMS) which plants are male sterile at low humidity and male fertile at high humidity. Previous studies have revealed that OsCER1 contributes to very-long-chain (VLC) alkanes biosynthesis in rice (Oryza sativa L.). Here, applying the CRISPR/Cas9 technique, we obtained two independent OsCER1 knockout lines (OsCER1Cas). Both OsCER1Cas lines exhibited HGMS. Mutant pollen showed defects in adhesion and germination on stigmas at low humidity, whereas high humidity enhanced the pollen germination rate. Transmission electron microscopy (TEM) observations of mutant pollen revealed abnormal tryphine structure, potentially representing the basis of HGMS. Furthermore, co-pollination with mixed OsCER1Cas mutant and maize (Zea mays L.) pollen could rescue the fertility of the mutant, thereby establishing the key role of tryphine in germination on stigmas. OsCER1 knockout might affect VLC alkane metabolism and therefore alter the lipid composition of tryphine. It could lead to the defects in pollen grain adhesion, hydration and germination, resulting in HGMS. This work identified the mechanism of HGMS induced by VLC alkanes in rice and the generality of tryphine in different species of Gramineae.

Environment‐sensitive genic male sterility in rice and other plants

“…Thus, the pollen grains dehydrate quite rapidly, in turn affecting the adhesion, hydration and germination of pollen grains on the stigma. This male sterility of these humidity‐sensitive genic male sterile lines can be rescued by increasing humidity (H. Chen et al, 2020; E. Ni et al, 2018, 2021; Xue et al, 2018; B. Yu et al, 2019) (Figure 8).…”

“…Ni et al, 2018). Deficiency of these very-long-chain fatty acids and their derivatives such as alkanes affects the formation of tryphine of the pollen wall (H. Chen et al, 2020;E. Ni et al, 2021).…”

“…Many genes regulating pollen-typed humidity-sensitive genic male sterility have been found to be related to the process of pollen wall synthesis, including Oxidosqualene cyclases (OsOSC12/OsPTS1), HUMIDITY-SENSITIVE GENIC MALE STERILITY 1 (HMS1), HMS1-INTERACTING PROTEIN (HMS1I) and OsCER1/OsGL1-4 in rice, and CER1, CER3, CER6, CER8 and CER10 in Arabidopsis (H. Chen et al, 2020;Koornneef et al, 1989;E. Ni et al, 2018E. Ni et al, , 2021Xue et al, 2018;B.…”

“…This male sterility of these humidity-sensitive genic male sterile lines can be rescued by increasing humidity (H. Chen et al, 2020;E. Ni et al, 2018E. Ni et al, , 2021Xue et al, 2018;B.…”

“…The pollen‐type humidity‐sensitive genic male sterility involves pollen grain dehydration being sensitive to humidity, whereas anther‐type humidity‐sensitive genic male sterility involves anther dehiscence being sensitive to humidity. Many genes regulating pollen‐typed humidity‐sensitive genic male sterility have been found to be related to the process of pollen wall synthesis, including Oxidosqualene cyclases ( OsOSC12 / OsPTS1 ), HUMIDITY‐SENSITIVE GENIC MALE STERILITY 1 ( HMS1 ), HMS1‐INTERACTING PROTEIN ( HMS1I ) and OsCER1 / OsGL1‐4 in rice, and CER1 , CER3 , CER6 , CER8 and CER10 in Arabidopsis (H. Chen et al, 2020; Koornneef et al, 1989; E. Ni et al, 2018, 2021; Xue et al, 2018; B. Yu et al, 2019). The mutation of INDUCER OF CBF EXPRESSION 1 ( ICE1 ) leads to anther‐type humidity‐sensitive genic male sterility (Wei et al, 2018).…”