GmTNRP1, associated with rhizobial type‐III effector NopT, regulates nitrogenase activity in the nodules of soybean (Glycine max)

Abstract Soybean is a rich source of protein and oil for humans. It forms a symbiotic association with rhizobia to fix atmospheric nitrogen for its growth and development. Rhizobial type‐III effectors act as important signaling molecules in symbiosis. However, they are poorly studied. In this study,...

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Main Authors: Chao Ma, Chunyan Liu, Yanyu Yu, Shengnan Ma, Siyang Pan, Haojie Feng, Qingshan Chen, Dawei Xin, Xiaoxia Wu, Jinhui Wang
Format: Article
Language:English
Published: Wiley 2023-07-01
Series:Food and Energy Security
Subjects:
Online Access:https://doi.org/10.1002/fes3.466
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author Chao Ma
Chunyan Liu
Yanyu Yu
Shengnan Ma
Siyang Pan
Haojie Feng
Qingshan Chen
Dawei Xin
Xiaoxia Wu
Jinhui Wang
author_facet Chao Ma
Chunyan Liu
Yanyu Yu
Shengnan Ma
Siyang Pan
Haojie Feng
Qingshan Chen
Dawei Xin
Xiaoxia Wu
Jinhui Wang
author_sort Chao Ma
collection DOAJ
description Abstract Soybean is a rich source of protein and oil for humans. It forms a symbiotic association with rhizobia to fix atmospheric nitrogen for its growth and development. Rhizobial type‐III effectors act as important signaling molecules in symbiosis. However, they are poorly studied. In this study, mutation of TtsI in Sinorhizobium fredii HH103 reduced nodule numbers and dry weights in SN14 (cultivated soybean) and ZYD00006 (wild soybean). Moreover, it reduced nitrogenase activity in SN14 but not in ZYD00006. Based on the differences in nitrogenase activity between SN14 and ZYD00006 inoculated with HH103 and the TtsI mutant, two conditional quantitative trait loci associated with nitrogenase activity were identified in chromosome segment substitution lines derived from SN14 and ZYD00006. Using transcriptome analysis, single‐nucleotide polymorphism (SNP) analysis, and qRT‐PCR, Glyma.13G150000 (GmTNRP1) was identified as a candidate gene in soybean that was associated with nitrogenase activity, along with NopT (a type‐III effector). In addition, GmTNRP1 (an LRR‐RK family protein located on the cell membrane) was observed to be induced by NopT to negatively regulate nitrogenase activity. In transgenic hairy roots with GmTNRP1 silencing, no significant difference was observed in terms of nitrogenase activity between nodules inoculated with the NopT mutant and those inoculated with HH103 (wild type). However, the nitrogenase activity in the nodules decreased after overexpression of GmTNRP1. SNP located in the GmTNRP1 promoter affected its expression in response to NopT. Haplotype analysis revealed that SN14 belonged to Hap1 and ZYD00006 belonged to Hap2, which explained the different results in the two varieties. To the best of our knowledge, this is the first study to identify a soybean gene associated with a rhizobial type‐III effector in the nodules. GmTNRP1 can negatively regulate nitrogenase activity in the nodules. This study enhanced the understanding of the mechanism underlying symbiotic association between soybean and rhizobia.
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spelling doaj.art-a31eea1a119840009d23262125b94a9c2023-07-20T06:37:10ZengWileyFood and Energy Security2048-36942023-07-01124n/an/a10.1002/fes3.466GmTNRP1, associated with rhizobial type‐III effector NopT, regulates nitrogenase activity in the nodules of soybean (Glycine max)Chao Ma0Chunyan Liu1Yanyu Yu2Shengnan Ma3Siyang Pan4Haojie Feng5Qingshan Chen6Dawei Xin7Xiaoxia Wu8Jinhui Wang9College of Agriculture, Key Laboratory of Soybean Biology in Chinese Ministry of Education Northeast Agricultural University Harbin ChinaCollege of Agriculture, Key Laboratory of Soybean Biology in Chinese Ministry of Education Northeast Agricultural University Harbin ChinaCollege of Agriculture, Key Laboratory of Soybean Biology in Chinese Ministry of Education Northeast Agricultural University Harbin ChinaCollege of Agriculture, Key Laboratory of Soybean Biology in Chinese Ministry of Education Northeast Agricultural University Harbin ChinaCollege of Agriculture, Key Laboratory of Soybean Biology in Chinese Ministry of Education Northeast Agricultural University Harbin ChinaCollege of Agriculture, Key Laboratory of Soybean Biology in Chinese Ministry of Education Northeast Agricultural University Harbin ChinaCollege of Agriculture, Key Laboratory of Soybean Biology in Chinese Ministry of Education Northeast Agricultural University Harbin ChinaCollege of Agriculture, Key Laboratory of Soybean Biology in Chinese Ministry of Education Northeast Agricultural University Harbin ChinaCollege of Agriculture, Key Laboratory of Soybean Biology in Chinese Ministry of Education Northeast Agricultural University Harbin ChinaCollege of Agriculture, Key Laboratory of Soybean Biology in Chinese Ministry of Education Northeast Agricultural University Harbin ChinaAbstract Soybean is a rich source of protein and oil for humans. It forms a symbiotic association with rhizobia to fix atmospheric nitrogen for its growth and development. Rhizobial type‐III effectors act as important signaling molecules in symbiosis. However, they are poorly studied. In this study, mutation of TtsI in Sinorhizobium fredii HH103 reduced nodule numbers and dry weights in SN14 (cultivated soybean) and ZYD00006 (wild soybean). Moreover, it reduced nitrogenase activity in SN14 but not in ZYD00006. Based on the differences in nitrogenase activity between SN14 and ZYD00006 inoculated with HH103 and the TtsI mutant, two conditional quantitative trait loci associated with nitrogenase activity were identified in chromosome segment substitution lines derived from SN14 and ZYD00006. Using transcriptome analysis, single‐nucleotide polymorphism (SNP) analysis, and qRT‐PCR, Glyma.13G150000 (GmTNRP1) was identified as a candidate gene in soybean that was associated with nitrogenase activity, along with NopT (a type‐III effector). In addition, GmTNRP1 (an LRR‐RK family protein located on the cell membrane) was observed to be induced by NopT to negatively regulate nitrogenase activity. In transgenic hairy roots with GmTNRP1 silencing, no significant difference was observed in terms of nitrogenase activity between nodules inoculated with the NopT mutant and those inoculated with HH103 (wild type). However, the nitrogenase activity in the nodules decreased after overexpression of GmTNRP1. SNP located in the GmTNRP1 promoter affected its expression in response to NopT. Haplotype analysis revealed that SN14 belonged to Hap1 and ZYD00006 belonged to Hap2, which explained the different results in the two varieties. To the best of our knowledge, this is the first study to identify a soybean gene associated with a rhizobial type‐III effector in the nodules. GmTNRP1 can negatively regulate nitrogenase activity in the nodules. This study enhanced the understanding of the mechanism underlying symbiotic association between soybean and rhizobia.https://doi.org/10.1002/fes3.466functional studynitrogenase activityQTLsoybeansymbiosistype‐III effector
spellingShingle Chao Ma
Chunyan Liu
Yanyu Yu
Shengnan Ma
Siyang Pan
Haojie Feng
Qingshan Chen
Dawei Xin
Xiaoxia Wu
Jinhui Wang
GmTNRP1, associated with rhizobial type‐III effector NopT, regulates nitrogenase activity in the nodules of soybean (Glycine max)
Food and Energy Security
functional study
nitrogenase activity
QTL
soybean
symbiosis
type‐III effector
title GmTNRP1, associated with rhizobial type‐III effector NopT, regulates nitrogenase activity in the nodules of soybean (Glycine max)
title_full GmTNRP1, associated with rhizobial type‐III effector NopT, regulates nitrogenase activity in the nodules of soybean (Glycine max)
title_fullStr GmTNRP1, associated with rhizobial type‐III effector NopT, regulates nitrogenase activity in the nodules of soybean (Glycine max)
title_full_unstemmed GmTNRP1, associated with rhizobial type‐III effector NopT, regulates nitrogenase activity in the nodules of soybean (Glycine max)
title_short GmTNRP1, associated with rhizobial type‐III effector NopT, regulates nitrogenase activity in the nodules of soybean (Glycine max)
title_sort gmtnrp1 associated with rhizobial type iii effector nopt regulates nitrogenase activity in the nodules of soybean glycine max
topic functional study
nitrogenase activity
QTL
soybean
symbiosis
type‐III effector
url https://doi.org/10.1002/fes3.466
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