Population genetics of the cereal cyst nematode Heterodera avenae reveal geographical segregation and host adaptation

Abstract Cereal cyst nematodes (CCNs) lead to major losses in the cereal crop industry worldwide and have been reported in many provinces of China. However, this plant nematode’s distribution and genetic differences are not fully understood. In the present study, 821 soil and host root samples were...

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Main Authors: Hudie Shao, Linfeng Zhu, Zhiqiang Li, Ru Jiang, Shiming Liu, Wenkun Huang, Chuanren Li, Ling-an Kong, Deliang Peng, Huan Peng
Format: Article
Language:English
Published: BMC 2023-07-01
Series:Phytopathology Research
Subjects:
Online Access:https://doi.org/10.1186/s42483-023-00185-x
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author Hudie Shao
Linfeng Zhu
Zhiqiang Li
Ru Jiang
Shiming Liu
Wenkun Huang
Chuanren Li
Ling-an Kong
Deliang Peng
Huan Peng
author_facet Hudie Shao
Linfeng Zhu
Zhiqiang Li
Ru Jiang
Shiming Liu
Wenkun Huang
Chuanren Li
Ling-an Kong
Deliang Peng
Huan Peng
author_sort Hudie Shao
collection DOAJ
description Abstract Cereal cyst nematodes (CCNs) lead to major losses in the cereal crop industry worldwide and have been reported in many provinces of China. However, this plant nematode’s distribution and genetic differences are not fully understood. In the present study, 821 soil and host root samples were collected from 16 provinces in 2019–2022 to investigate the distribution of the CCNs. Heterodera avenae was detected in 56.39% of the total samples, primarily in Hubei, Henan, Hebei, Shandong, Shanxi, Gansu, Beijing, Tianjin, Inner Mongolia, Ningxia, Xinjiang, Qinghai, Anhui, Shaanxi, and Jiangsu. H. filipjevi was present in 21 samples, with a detection rate of 2.60%, and it was found mainly in Henan, Anhui, Jiangsu, Shandong, Shanxi, and Qinghai. A phylogenetic analysis of the internal transcribed spacer (ITS) region of the rRNA gene indicated that significant evolutionary and genetic differences existed between the Chinese populations and populations from other countries. Our results indicate that ITS1 can be used as a phylogenetic analysis and genetic target for H. avenae populations. The haplotypes of the ITS1 sequences of H. avenae populations from 14 countries were analyzed, and we speculate that H. avenae originated in a Middle East hotspot, then spread westwards to Europe and the United States and eastwards to China and Australia. Genetic differences between Asian and European populations suggest that the Himalayas and Kunlun Mountains formed a barrier that resulted in the formation of a separate evolutionary group in China. The phylogenetic and haplotype analysis results from different hosts showed significant differences among populations isolated from different hosts, and those isolated from weeds were distinct from those from other hosts, indicating that the rich genetic diversity of H. avenae populations is related to the large number of available hosts. Above all, geographic barriers, time of origin, and host adaptation might explain the current known distribution patterns of Chinese H. avenae populations.
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spelling doaj.art-953c62983beb48c49041f6903b085de52023-07-09T11:07:58ZengBMCPhytopathology Research2524-41672023-07-015111310.1186/s42483-023-00185-xPopulation genetics of the cereal cyst nematode Heterodera avenae reveal geographical segregation and host adaptationHudie Shao0Linfeng Zhu1Zhiqiang Li2Ru Jiang3Shiming Liu4Wenkun Huang5Chuanren Li6Ling-an Kong7Deliang Peng8Huan Peng9State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesAgricultural Information Institute, Chinese Academy of Agricultural SciencesAdsen Biotechnology Co., Ltd.State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesCollege of Agriculture, Yangtze UniversityState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesAbstract Cereal cyst nematodes (CCNs) lead to major losses in the cereal crop industry worldwide and have been reported in many provinces of China. However, this plant nematode’s distribution and genetic differences are not fully understood. In the present study, 821 soil and host root samples were collected from 16 provinces in 2019–2022 to investigate the distribution of the CCNs. Heterodera avenae was detected in 56.39% of the total samples, primarily in Hubei, Henan, Hebei, Shandong, Shanxi, Gansu, Beijing, Tianjin, Inner Mongolia, Ningxia, Xinjiang, Qinghai, Anhui, Shaanxi, and Jiangsu. H. filipjevi was present in 21 samples, with a detection rate of 2.60%, and it was found mainly in Henan, Anhui, Jiangsu, Shandong, Shanxi, and Qinghai. A phylogenetic analysis of the internal transcribed spacer (ITS) region of the rRNA gene indicated that significant evolutionary and genetic differences existed between the Chinese populations and populations from other countries. Our results indicate that ITS1 can be used as a phylogenetic analysis and genetic target for H. avenae populations. The haplotypes of the ITS1 sequences of H. avenae populations from 14 countries were analyzed, and we speculate that H. avenae originated in a Middle East hotspot, then spread westwards to Europe and the United States and eastwards to China and Australia. Genetic differences between Asian and European populations suggest that the Himalayas and Kunlun Mountains formed a barrier that resulted in the formation of a separate evolutionary group in China. The phylogenetic and haplotype analysis results from different hosts showed significant differences among populations isolated from different hosts, and those isolated from weeds were distinct from those from other hosts, indicating that the rich genetic diversity of H. avenae populations is related to the large number of available hosts. Above all, geographic barriers, time of origin, and host adaptation might explain the current known distribution patterns of Chinese H. avenae populations.https://doi.org/10.1186/s42483-023-00185-xCereal cyst nematodeDistributionHaplotypeGeographic barrierHost adaptation
spellingShingle Hudie Shao
Linfeng Zhu
Zhiqiang Li
Ru Jiang
Shiming Liu
Wenkun Huang
Chuanren Li
Ling-an Kong
Deliang Peng
Huan Peng
Population genetics of the cereal cyst nematode Heterodera avenae reveal geographical segregation and host adaptation
Phytopathology Research
Cereal cyst nematode
Distribution
Haplotype
Geographic barrier
Host adaptation
title Population genetics of the cereal cyst nematode Heterodera avenae reveal geographical segregation and host adaptation
title_full Population genetics of the cereal cyst nematode Heterodera avenae reveal geographical segregation and host adaptation
title_fullStr Population genetics of the cereal cyst nematode Heterodera avenae reveal geographical segregation and host adaptation
title_full_unstemmed Population genetics of the cereal cyst nematode Heterodera avenae reveal geographical segregation and host adaptation
title_short Population genetics of the cereal cyst nematode Heterodera avenae reveal geographical segregation and host adaptation
title_sort population genetics of the cereal cyst nematode heterodera avenae reveal geographical segregation and host adaptation
topic Cereal cyst nematode
Distribution
Haplotype
Geographic barrier
Host adaptation
url https://doi.org/10.1186/s42483-023-00185-x
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