Host-induced silencing of a nematode chitin synthase gene decreases abundance of rhizosphere fungal community while enhancing Heterodera glycines resistance of soybean
Shuan Tian A # , Xue Shi A # , Baoyuan Qu B , Houxiang Kang A , Wenkun Huang A , Huan Peng A , Deliang Peng
A , Jiajun Wang C , Shiming Liu A * and Lingan Kong A *
+ Author Affiliations
- Author Affiliations
A State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China.
B State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
C Institute of Soybean Research, Heilongjiang Academy of Agricultural Sciences, Harbin 150086, China.
* Correspondence to: liushiming01@caas.cn, konglingan@caas.cn
# These authors contributed equally to this paper
Handling Editor: Marta Santalla
Crop & Pasture Science 73(10) 1156-1167 https://doi.org/10.1071/CP22030
Submitted: 14 December 2021 Accepted: 10 March 2022 Published: 23 April 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Context: A transgenic variety of soybean (Glycine max (L.) Merr.), H57, has been developed from wild-type variety Jack, with host-induced gene silencing of a chitin synthase gene (CHS) in soybean cyst nematode (SCN, Heterodera glycines Ichinohe), a devastating pathogen in soybean. H57 needs to be characterised for suitability to manage SCN, especially because rhizosphere microbial communities may be sensitive to genetically modified crops.
Aims: We aimed to evaluate the SCN resistance of H57 at the T7 generation, and analyse the impact on the rhizosphere microbial community of planting H57 into SCN-infected soil.
Methods: Infection with SCN was assessed at 60 days after planting of H57 and Jack into SCN-infected soil by examining recovered cysts from rhizosphere soil and comparing with an infected bulk soil control. For analysis of rhizosphere microbial communities (bacterial and fungal), 16S and ITS amplicons were identified by high-throughput sequencing, and bioinformatic analysis was used to define operational taxonomic units. Alpha diversity, using five indexes, and relative abundance were determined.
Key results: Soybean H57 showed significantly enhanced and heritable resistance to SCN compared with Jack. The diversity and richness (abundance) of the bacterial community of H57 and Jack were significantly and similarly increased relative to the bulk soil. The fungal community of H57 had considerably lower abundance than both other treatments, and lower diversity than the bulk soil. The relative abundance of only two bacterial phyla (Acidobacteria and Actinobacteria) and one fungal phylum (Glomeromycota), and three bacterial genera (Candidatus_Solibacter, Candidatus_Udaeobacter and Bryobacter) and one fungal genus (Aspergillus), differed significantly between rhizosphere soils of H57 and Jack.
Conclusions: Host-induced gene silencing of SCN-CHS substantially and heritably enhanced SCN resistance in soybean, did not significantly alter the rhizosphere bacterial community, but greatly suppressed the abundance of the rhizosphere fungal community, which was likely associated with boosted SCN resistance.
Implications: This study established a basis for interaction research between soybean with SCN-CHS host-induced gene silencing and the rhizosphere microbial community, and for potentially planting soybean H57 to manage SCN.
Keywords: abundance, chitin synthase, diversity, host-induced silencing of gene, rhizosphere microbial community, SCN resistance, soybean, transgenic soybean H57.
References
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120.| Trimmomatic: a flexible trimmer for Illumina sequence data.Crossref | GoogleScholarGoogle Scholar | 24695404PubMed |
Brundrett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytologist 220, 1108–1115.
| Evolutionary history of mycorrhizal symbioses and global host plant diversity.Crossref | GoogleScholarGoogle Scholar |
Caporaso JG, Kuczynski J, Stombaugh J, et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7, 335–336.
| QIIME allows analysis of high-throughput community sequencing data.Crossref | GoogleScholarGoogle Scholar | 20383131PubMed |
Chaudhary S, Dutta TK, Tyagi N, Shivakumara TN, Papolu PK, Chobhe KA, Rao U (2019) Host-induced silencing of Mi-msp-1 confers resistance to root-knot nematode Meloidogyne incognita in eggplant. Transgenic Research 28, 327–340.
| Host-induced silencing of Mi-msp-1 confers resistance to root-knot nematode Meloidogyne incognita in eggplant.Crossref | GoogleScholarGoogle Scholar | 30955133PubMed |
Chauhan A, Smartt A, Wang J, et al. (2014) Integrated metagenomics and metatranscriptomics analyses of root-associated soil from transgenic switchgrass. Genome Announcements 2, e00777-14
| Integrated metagenomics and metatranscriptomics analyses of root-associated soil from transgenic switchgrass.Crossref | GoogleScholarGoogle Scholar | 25125642PubMed |
Cheng W, Song XS, Li HP, Cao LH, Sun K, Qiu XL, Xu YB, Yang P, Huang T, Zhang JB, Qu B, Liao YC (2015) Host-induced gene silencing of an essential chitin synthase gene confers durable resistance to Fusarium head blight and seedling blight in wheat. Plant Biotechnology Journal 13, 1335–1345.
| Host-induced gene silencing of an essential chitin synthase gene confers durable resistance to Fusarium head blight and seedling blight in wheat.Crossref | GoogleScholarGoogle Scholar | 25735638PubMed |
Edgar R (2017) SEARCH_16S: a new algorithm for identifying 16S ribosomal RNA genes in contigs and chromosomes. BioRxiv
| SEARCH_16S: a new algorithm for identifying 16S ribosomal RNA genes in contigs and chromosomes.Crossref | GoogleScholarGoogle Scholar |
Filion M (2008) Do transgenic plants affect rhizobacteria populations? Microbial Biotechnology 1, 463–475.
| Do transgenic plants affect rhizobacteria populations?Crossref | GoogleScholarGoogle Scholar | 21261867PubMed |
Gao N, Shen W, Lin X, Shi W (2015) Influence of transgenic ath-miR399d tomato lines on microbial community and diversity in rhizosphere soil. Soil Science and Plant Nutrition 61, 259–268.
| Influence of transgenic ath-miR399d tomato lines on microbial community and diversity in rhizosphere soil.Crossref | GoogleScholarGoogle Scholar |
Jin N, Liu SM, Peng H, Huang WK, Kong LA, Wu YH, Chen Y, Ge FY, Jian H, Peng DL (2019) Isolation and characterization of Aspergillus niger NBC001 underlying suppression against Heterodera glycines. Scientific Reports 9, 591
| Isolation and characterization of Aspergillus niger NBC001 underlying suppression against Heterodera glycines.Crossref | GoogleScholarGoogle Scholar | 30679719PubMed |
Jin N, Liu SM, Peng H, Huang WK, Kong LA, Peng DL (2021) Effect of Aspergillus niger NBC001 on the soybean rhizosphere microbial community in a soybean cyst nematode-infested field. Journal of Integrative Agriculture 20, 3230–3239.
| Effect of Aspergillus niger NBC001 on the soybean rhizosphere microbial community in a soybean cyst nematode-infested field.Crossref | GoogleScholarGoogle Scholar |
Kielak AM, Barreto CC, Kowalchuk GA, van Veen JA, Kuramae EE (2016) The ecology of Acidobacteria: moving beyond genes and genomics. Frontiers in Microbiology 7, 744
| The ecology of Acidobacteria: moving beyond genes and genomics.Crossref | GoogleScholarGoogle Scholar | 27303369PubMed |
Kim KS, Vuong TD, Qiu D, Robbins RT, Grover Shannon J, Li Z, Nguyen HT (2016) Advancements in breeding, genetics, and genomics for resistance to three nematode species in soybean. Theoretical and Applied Genetics 129, 2295–2311.
| Advancements in breeding, genetics, and genomics for resistance to three nematode species in soybean.Crossref | GoogleScholarGoogle Scholar | 27796432PubMed |
Kong LA, Yang J, Li GT, Qi LL, Zhang YJ, Wang CF, Zhao WS, Xu JR, Peng YL (2012) Different chitin synthase genes are required for various developmental and plant infection processes in the rice blast fungus Magnaporthe oryzae. PLoS Pathogens 8, e1002526
| Different chitin synthase genes are required for various developmental and plant infection processes in the rice blast fungus Magnaporthe oryzae.Crossref | GoogleScholarGoogle Scholar | 22346755PubMed |
Kong L, Shi X, Chen D, Yang N, Yin C, Yang J, Wang G, Huang G, Peng H, Peng D, Liu S (2022) Host-induced silencing of a nematode chitin synthase gene enhances resistance of soybeans to both pathogenic Heterodera glycines and Fusarium oxysporum. Plant Biotechnology Journal
| Host-induced silencing of a nematode chitin synthase gene enhances resistance of soybeans to both pathogenic Heterodera glycines and Fusarium oxysporum.Crossref | GoogleScholarGoogle Scholar | 35301818PubMed |
Kostov K, Krogh PH, Damgaard CF (2014) Are soil microbial endpoints changed by Bt crops compared with conventional crops? A systematic review protocol. Environmental Evidence 3, 11
| Are soil microbial endpoints changed by Bt crops compared with conventional crops? A systematic review protocol.Crossref | GoogleScholarGoogle Scholar |
Lee SI, Lee KJ, Chun HH, Ha S, Gwak HJ, Kim HM, Lee JH, Choi HJ, Kim HH, Shin TS, Park HW, Kim JC (2018) Process development of oxalic acid production in submerged culture of Aspergillus niger F22 and its biocontrol efficacy against the root-knot nematode Meloidogyne incognita. Bioprocess and Biosystems Engineering 41, 345–352.
| Process development of oxalic acid production in submerged culture of Aspergillus niger F22 and its biocontrol efficacy against the root-knot nematode Meloidogyne incognita.Crossref | GoogleScholarGoogle Scholar | 29150701PubMed |
Li J, Todd TC, Oakley TR, Lee J, Trick HN (2010) Host-derived suppression of nematode reproductive and fitness genes decreases fecundity of Heterodera glycines Ichinohe. Planta 232, 775–785.
| Host-derived suppression of nematode reproductive and fitness genes decreases fecundity of Heterodera glycines Ichinohe.Crossref | GoogleScholarGoogle Scholar | 20582434PubMed |
Liang J, Jiao Y, Luan Y, Sun S, Wu C, Wu H, Zhang M, Zhang H, Zheng X, Zhang Z (2018) A 2-year field trial reveals no significant effects of GM high-methionine soybean on the rhizosphere bacterial communities. World Journal of Microbiology and Biotechnology 34, 113
| A 2-year field trial reveals no significant effects of GM high-methionine soybean on the rhizosphere bacterial communities.Crossref | GoogleScholarGoogle Scholar | 29987404PubMed |
Liu Y, Ding Z, Peng DL, Liu SM, Kong LA, Peng H, Xiang C, Li ZC, Huang WK (2019) Evaluation of the biocontrol potential of Aspergillus welwitschiae against the root-knot nematode Meloidogyne graminicola in rice (Oryza sativa L.). Journal of Integrative Agriculture 18, 2561–2570.
| Evaluation of the biocontrol potential of Aspergillus welwitschiae against the root-knot nematode Meloidogyne graminicola in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar |
Lladó S, Žifčáková L, Větrovský T, Eichlerová I, Baldrian P (2016) Functional screening of abundant bacteria from acidic forest soil indicates the metabolic potential of Acidobacteria subdivision 1 for polysaccharide decomposition. Biology and Fertility of Soils 52, 251–260.
| Functional screening of abundant bacteria from acidic forest soil indicates the metabolic potential of Acidobacteria subdivision 1 for polysaccharide decomposition.Crossref | GoogleScholarGoogle Scholar |
Mao YB, Cai WJ, Wang JW, Hong GJ, Tao XY, Wang LJ, Huang YP, Chen XY (2007) Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nature Biotechnology 25, 1307–1313.
| Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol.Crossref | GoogleScholarGoogle Scholar | 17982444PubMed |
Niblack TL, Lambert KN, Tylka GL (2006) A model plant pathogen from the kingdom Animalia: Heterodera glycines, the soybean cyst nematode. Annual Review of Phytopathology 44, 283–303.
| A model plant pathogen from the kingdom Animalia: Heterodera glycines, the soybean cyst nematode.Crossref | GoogleScholarGoogle Scholar | 16704359PubMed |
Nowara D, Gay A, Lacomme C, Shaw J, Ridout C, Douchkov D, Hensel G, Kumlehn J, Schweizer P (2010) HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. The Plant Cell 22, 3130–3141.
| HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis.Crossref | GoogleScholarGoogle Scholar | 20884801PubMed |
Peng D, Jiang R, Peng H, Liu S (2021) Soybean cyst nematodes: a destructive threat to soybean production in China. Phytopathology Research 3, 19
| Soybean cyst nematodes: a destructive threat to soybean production in China.Crossref | GoogleScholarGoogle Scholar |
Shaibu AS, Li B, Zhang S, Sun J (2020) Soybean cyst nematode-resistance: gene identification and breeding strategies. The Crop Journal 8, 892–904.
| Soybean cyst nematode-resistance: gene identification and breeding strategies.Crossref | GoogleScholarGoogle Scholar |
Shemshura ON, Bekmakhanova NE, Mazunina MN, Meyer SLF, Rice CP, Masler EP (2016) Isolation and identification of nematode-antagonistic compounds from the fungus Aspergillus candidus. FEMS Microbiology Letters 363, fnw026
| Isolation and identification of nematode-antagonistic compounds from the fungus Aspergillus candidus.Crossref | GoogleScholarGoogle Scholar | 26850440PubMed |
Shivakumara TN, Chaudhary S, Kamaraju D, Dutta TK, Papolu PK, Banakar P, Sreevathsa R, Singh B, Manjaiah KM, Rao U (2017) Host-induced silencing of two pharyngeal gland genes conferred transcriptional alteration of cell wall-modifying enzymes of Meloidogyne incognita vis-à-vis perturbed nematode infectivity in eggplant. Frontiers in Plant Science 8, 473
| Host-induced silencing of two pharyngeal gland genes conferred transcriptional alteration of cell wall-modifying enzymes of Meloidogyne incognita vis-à-vis perturbed nematode infectivity in eggplant.Crossref | GoogleScholarGoogle Scholar | 28424727PubMed |
Singh BK, Millard P, Whiteley AS, Murrell JC (2004) Unravelling rhizosphere-microbial interactions: opportunities and limitations. Trends in Microbiology 12, 386–393.
| Unravelling rhizosphere-microbial interactions: opportunities and limitations.Crossref | GoogleScholarGoogle Scholar | 15276615PubMed |
Stürmer SL, Kemmelmeier K, Moreira BC, Kasuya MCM, Pereira GMD, da Silva K (2018) Arbuscular mycorrhizal fungi (Glomeromycota) communities in tropical savannas of Roraima, Brazil. Mycological Progress 17, 1149–1159.
| Arbuscular mycorrhizal fungi (Glomeromycota) communities in tropical savannas of Roraima, Brazil.Crossref | GoogleScholarGoogle Scholar |
Tian B, Li J, Oakley TR, Todd TC, Trick HN (2016) Host-derived artificial microRNA as an alternative method to improve soybean resistance to soybean cyst nematode. Genes 7, 122
| Host-derived artificial microRNA as an alternative method to improve soybean resistance to soybean cyst nematode.Crossref | GoogleScholarGoogle Scholar |
Ward NL, Challacombe JF, Janssen PH, et al. (2009) Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Applied and Environmental Microbiology 75, 2046–2056.
| Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils.Crossref | GoogleScholarGoogle Scholar | 19201974PubMed |
Wu J, Yu M, Xu J, Du J, Ji F, Dong F, Li X, Shi J (2014) Impact of transgenic wheat with wheat yellow mosaic virus resistance on microbial community diversity and enzyme activity in rhizosphere soil. PLoS ONE 9, e98394
| Impact of transgenic wheat with wheat yellow mosaic virus resistance on microbial community diversity and enzyme activity in rhizosphere soil.Crossref | GoogleScholarGoogle Scholar | 24897124PubMed |
Zhang T, Jin Y, Zhao JH, Gao F, Zhou BJ, Fang YY, Guo HS (2016) Host-induced gene silencing of the target gene in fungal cells confers effective resistance to the cotton wilt disease pathogen Verticillium dahliae. Molecular Plant 9, 939–942.
| Host-induced gene silencing of the target gene in fungal cells confers effective resistance to the cotton wilt disease pathogen Verticillium dahliae.Crossref | GoogleScholarGoogle Scholar | 26925819PubMed |
