The Rice Qa-SNAREs in SYP13 Subfamily Are Involved in Regulating Arbuscular Mycorrhizal Symbiosis and Seed Fertility

Qa-SNARE gene SYP132 (isoform α) was previously reported to affect arbuscular mycorrhizal (AM) symbiosis in the legume species Medicago truncatula. In non-legumes especially monocots, it remains unknown whether certain SNARE genes are also involved in AM symbiosis. In this work, we studied a rice or...

Full description

Bibliographic Details
Main Authors: Ying-Na Liu, Cheng-Chen Liu, Rui Guo, Li Tian, Jian-Fei Cheng, Ya-Nan Wu, Dong Wang, Bin Wang
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-05-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.898286/full
_version_ 1828815826953699328
author Ying-Na Liu
Cheng-Chen Liu
Rui Guo
Li Tian
Jian-Fei Cheng
Ya-Nan Wu
Dong Wang
Bin Wang
author_facet Ying-Na Liu
Cheng-Chen Liu
Rui Guo
Li Tian
Jian-Fei Cheng
Ya-Nan Wu
Dong Wang
Bin Wang
author_sort Ying-Na Liu
collection DOAJ
description Qa-SNARE gene SYP132 (isoform α) was previously reported to affect arbuscular mycorrhizal (AM) symbiosis in the legume species Medicago truncatula. In non-legumes especially monocots, it remains unknown whether certain SNARE genes are also involved in AM symbiosis. In this work, we studied a rice orthologous gene OsSYP132, which showed induced expression in mycorrhizal roots and two paralogous genes OsSYP131a and OsSYP131b, which were not induced by the AM fungus Rhizophagus irregularis. After employing CRISPR/Cas9 technique to generate their mutants, the Ossyp131a homozygous mutant T0 plants exhibited a dwarf phenotype and produced no fertile seeds, indicating a required role of this gene in seed fertility. Unlike the case in legume, the Ossyp132 mutants exhibited normal mycorrhizal phenotype, so did the Ossyp131b mutants. In the Ossyp131b Ossyp132 double mutants, however, the colonization rate and arbuscule abundance level decreased markedly, indicating an impaired fungal proliferation ability in rice roots. Such a defect was further confirmed by the reduced expression levels of AM marker genes. Our results in rice therefore demonstrated that while SYP13II members showed evolutionary and induction patterns specific to symbiosis, AM symbiosis is in fact controlled by the combined action of both SYP13I and SYP13II clades, revealing a functional redundancy among SYNTAXIN genes in mutualism.
first_indexed 2024-12-12T10:51:50Z
format Article
id doaj.art-79da29531c3d43a79c359f4988449b76
institution Directory Open Access Journal
issn 1664-462X
language English
last_indexed 2024-12-12T10:51:50Z
publishDate 2022-05-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Plant Science
spelling doaj.art-79da29531c3d43a79c359f4988449b762022-12-22T00:26:45ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-05-011310.3389/fpls.2022.898286898286The Rice Qa-SNAREs in SYP13 Subfamily Are Involved in Regulating Arbuscular Mycorrhizal Symbiosis and Seed FertilityYing-Na Liu0Cheng-Chen Liu1Rui Guo2Li Tian3Jian-Fei Cheng4Ya-Nan Wu5Dong Wang6Bin Wang7Department of Biology, School of Life Sciences, Nanjing University, Nanjing, ChinaDepartment of Biology, School of Life Sciences, Nanjing University, Nanjing, ChinaDepartment of Biology, School of Life Sciences, Nanjing University, Nanjing, ChinaDepartment of Biology, School of Life Sciences, Nanjing University, Nanjing, ChinaDepartment of Biology, School of Life Sciences, Nanjing University, Nanjing, ChinaDepartment of Biology, School of Life Sciences, Nanjing University, Nanjing, ChinaDepartment of Biochemistry and Molecular Biology, University of Massachusetts Amherst, Amherst, MA, United StatesDepartment of Biology, School of Life Sciences, Nanjing University, Nanjing, ChinaQa-SNARE gene SYP132 (isoform α) was previously reported to affect arbuscular mycorrhizal (AM) symbiosis in the legume species Medicago truncatula. In non-legumes especially monocots, it remains unknown whether certain SNARE genes are also involved in AM symbiosis. In this work, we studied a rice orthologous gene OsSYP132, which showed induced expression in mycorrhizal roots and two paralogous genes OsSYP131a and OsSYP131b, which were not induced by the AM fungus Rhizophagus irregularis. After employing CRISPR/Cas9 technique to generate their mutants, the Ossyp131a homozygous mutant T0 plants exhibited a dwarf phenotype and produced no fertile seeds, indicating a required role of this gene in seed fertility. Unlike the case in legume, the Ossyp132 mutants exhibited normal mycorrhizal phenotype, so did the Ossyp131b mutants. In the Ossyp131b Ossyp132 double mutants, however, the colonization rate and arbuscule abundance level decreased markedly, indicating an impaired fungal proliferation ability in rice roots. Such a defect was further confirmed by the reduced expression levels of AM marker genes. Our results in rice therefore demonstrated that while SYP13II members showed evolutionary and induction patterns specific to symbiosis, AM symbiosis is in fact controlled by the combined action of both SYP13I and SYP13II clades, revealing a functional redundancy among SYNTAXIN genes in mutualism.https://www.frontiersin.org/articles/10.3389/fpls.2022.898286/fullrice (Oryza sativa)arbuscular mycorrhiza (AM)SNAREOsSYP13functional redundancy
spellingShingle Ying-Na Liu
Cheng-Chen Liu
Rui Guo
Li Tian
Jian-Fei Cheng
Ya-Nan Wu
Dong Wang
Bin Wang
The Rice Qa-SNAREs in SYP13 Subfamily Are Involved in Regulating Arbuscular Mycorrhizal Symbiosis and Seed Fertility
Frontiers in Plant Science
rice (Oryza sativa)
arbuscular mycorrhiza (AM)
SNARE
OsSYP13
functional redundancy
title The Rice Qa-SNAREs in SYP13 Subfamily Are Involved in Regulating Arbuscular Mycorrhizal Symbiosis and Seed Fertility
title_full The Rice Qa-SNAREs in SYP13 Subfamily Are Involved in Regulating Arbuscular Mycorrhizal Symbiosis and Seed Fertility
title_fullStr The Rice Qa-SNAREs in SYP13 Subfamily Are Involved in Regulating Arbuscular Mycorrhizal Symbiosis and Seed Fertility
title_full_unstemmed The Rice Qa-SNAREs in SYP13 Subfamily Are Involved in Regulating Arbuscular Mycorrhizal Symbiosis and Seed Fertility
title_short The Rice Qa-SNAREs in SYP13 Subfamily Are Involved in Regulating Arbuscular Mycorrhizal Symbiosis and Seed Fertility
title_sort rice qa snares in syp13 subfamily are involved in regulating arbuscular mycorrhizal symbiosis and seed fertility
topic rice (Oryza sativa)
arbuscular mycorrhiza (AM)
SNARE
OsSYP13
functional redundancy
url https://www.frontiersin.org/articles/10.3389/fpls.2022.898286/full
work_keys_str_mv AT yingnaliu thericeqasnaresinsyp13subfamilyareinvolvedinregulatingarbuscularmycorrhizalsymbiosisandseedfertility
AT chengchenliu thericeqasnaresinsyp13subfamilyareinvolvedinregulatingarbuscularmycorrhizalsymbiosisandseedfertility
AT ruiguo thericeqasnaresinsyp13subfamilyareinvolvedinregulatingarbuscularmycorrhizalsymbiosisandseedfertility
AT litian thericeqasnaresinsyp13subfamilyareinvolvedinregulatingarbuscularmycorrhizalsymbiosisandseedfertility
AT jianfeicheng thericeqasnaresinsyp13subfamilyareinvolvedinregulatingarbuscularmycorrhizalsymbiosisandseedfertility
AT yananwu thericeqasnaresinsyp13subfamilyareinvolvedinregulatingarbuscularmycorrhizalsymbiosisandseedfertility
AT dongwang thericeqasnaresinsyp13subfamilyareinvolvedinregulatingarbuscularmycorrhizalsymbiosisandseedfertility
AT binwang thericeqasnaresinsyp13subfamilyareinvolvedinregulatingarbuscularmycorrhizalsymbiosisandseedfertility
AT yingnaliu riceqasnaresinsyp13subfamilyareinvolvedinregulatingarbuscularmycorrhizalsymbiosisandseedfertility
AT chengchenliu riceqasnaresinsyp13subfamilyareinvolvedinregulatingarbuscularmycorrhizalsymbiosisandseedfertility
AT ruiguo riceqasnaresinsyp13subfamilyareinvolvedinregulatingarbuscularmycorrhizalsymbiosisandseedfertility
AT litian riceqasnaresinsyp13subfamilyareinvolvedinregulatingarbuscularmycorrhizalsymbiosisandseedfertility
AT jianfeicheng riceqasnaresinsyp13subfamilyareinvolvedinregulatingarbuscularmycorrhizalsymbiosisandseedfertility
AT yananwu riceqasnaresinsyp13subfamilyareinvolvedinregulatingarbuscularmycorrhizalsymbiosisandseedfertility
AT dongwang riceqasnaresinsyp13subfamilyareinvolvedinregulatingarbuscularmycorrhizalsymbiosisandseedfertility
AT binwang riceqasnaresinsyp13subfamilyareinvolvedinregulatingarbuscularmycorrhizalsymbiosisandseedfertility