<i>Epichloë</i> Endophyte Alters Bacterial Nitrogen-Cycling Gene Abundance in the Rhizosphere Soil of Perennial Ryegrass

Perennial ryegrass (<i data-eusoft-scrollable-element="1">Lolium perenne</i>), an important forage and turfgrass species, can establish a mutualistic symbiosis with the fungal endophyte <i data-eusoft-scrollable-element="1">Epichloë festucae</i> var. <i...

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Main Authors: Munire Maimaitiyiming, Yanxiang Huang, Letian Jia, Mofan Wu, Zhenjiang Chen
Format: Article
Language:English
Published: MDPI AG 2025-07-01
Series:Biology
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Online Access:https://www.mdpi.com/2079-7737/14/7/879
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author Munire Maimaitiyiming
Yanxiang Huang
Letian Jia
Mofan Wu
Zhenjiang Chen
author_facet Munire Maimaitiyiming
Yanxiang Huang
Letian Jia
Mofan Wu
Zhenjiang Chen
author_sort Munire Maimaitiyiming
collection DOAJ
description Perennial ryegrass (<i data-eusoft-scrollable-element="1">Lolium perenne</i>), an important forage and turfgrass species, can establish a mutualistic symbiosis with the fungal endophyte <i data-eusoft-scrollable-element="1">Epichloë festucae</i> var. <i data-eusoft-scrollable-element="1">lolii.</i> Although the physiological and ecological impacts of endophyte infection on ryegrass have been extensively investigated, the response of the soil microbial community and nitrogen-cycling gene to this relationship has received much less attention. The present study emphasized abundance and diversity variation in the AOB-<i data-eusoft-scrollable-element="1">amoA</i>, <i data-eusoft-scrollable-element="1">nirK</i> and <i data-eusoft-scrollable-element="1">nosZ</i> functional genes in the rhizosphere soil of the endophyte–ryegrass symbiosis following litter addition. We sampled four times: at T<sub data-eusoft-scrollable-element="1">0</sub> (prior to first litter addition), T<sub data-eusoft-scrollable-element="1">1</sub> (post 120 d of 1st litter addition), T<sub data-eusoft-scrollable-element="1">2</sub> (post 120 d of 2nd litter addition) and T<sub data-eusoft-scrollable-element="1">3</sub> (post 120 d of 3rd litter addition) times. Real-time fluorescence quantitative PCR (qPCR) and PCR amplification and sequencing were used to characterize the abundance and diversity of the AOB-<i data-eusoft-scrollable-element="1">amoA</i>, <i data-eusoft-scrollable-element="1">nirK</i> and <i data-eusoft-scrollable-element="1">nosZ</i> genes in rhizosphere soils of endophyte-infected (E+) plants and endophyte-free (E−) plants. A significant enhancement of total Phosphorus (P), Soil Organic Carbon (SOC), Ammonium ion (NH<sub data-eusoft-scrollable-element="1">4</sub><sup data-eusoft-scrollable-element="1">+</sup>) and Nitrate ion (NO<sub data-eusoft-scrollable-element="1">3</sub><sup data-eusoft-scrollable-element="1">−</sup>) contents in the rhizosphere soil was recorded in endophyte-infected plants at different sampling times compared to endophyte-free plants (<i data-eusoft-scrollable-element="1">p</i> ≤ 0.05). The absolute abundance of the AOB-<i data-eusoft-scrollable-element="1">amoA</i> gene at T<sub data-eusoft-scrollable-element="1">0</sub> and T<sub data-eusoft-scrollable-element="1">1</sub> times was higher, as was the absolute abundance of the <i data-eusoft-scrollable-element="1">nosZ</i> gene at T<sub data-eusoft-scrollable-element="1">0</sub>, T<sub data-eusoft-scrollable-element="1">1</sub> and T<sub data-eusoft-scrollable-element="1">3</sub> times in the E+ plant rhizophere soils relative to E− plant rhizosphere soils. A significant change in relative abundance of the AOB-<i data-eusoft-scrollable-element="1">amoA</i> and <i data-eusoft-scrollable-element="1">nosZ</i> genes in the host rhizophere soils of endophyte-infected plants at T<sub data-eusoft-scrollable-element="1">1</sub> and T<sub data-eusoft-scrollable-element="1">3</sub> times was observed. The experiment failed to show any significant alteration in abundance and diversity of the <i data-eusoft-scrollable-element="1">nirK</i> gene, and diversity of the AOB-<i data-eusoft-scrollable-element="1">amoA</i> and <i data-eusoft-scrollable-element="1">nosZ</i> genes. Analysis of the abundance and diversity of the <i data-eusoft-scrollable-element="1">nirK</i> gene indicated that changes in soil properties accounted for approximately 70.38% of the variation along the first axis and 16.69% along the second axis, and soil NH<sub data-eusoft-scrollable-element="1">4</sub><sup data-eusoft-scrollable-element="1">+</sup> (<i data-eusoft-scrollable-element="1">p</i> = 0.002, 50.4%) and soil C/P ratio (<i data-eusoft-scrollable-element="1">p</i> = 0.012, 15.8%) had a strong effect. The changes in community abundance and diversity of the AOB-<i data-eusoft-scrollable-element="1">amoA</i> and <i data-eusoft-scrollable-element="1">nosZ</i> genes were mainly related to soil pH, N/P ratio and NH<sub data-eusoft-scrollable-element="1">4</sub><sup data-eusoft-scrollable-element="1">+</sup> content. The results demonstrate that the existence of tripartite interactions among the foliar endophyte <i data-eusoft-scrollable-element="1">E</i>. <i data-eusoft-scrollable-element="1">festucae</i> var. <i data-eusoft-scrollable-element="1">Lolii</i>, <i data-eusoft-scrollable-element="1">L. perenne</i> and soil nitrogen-cycling gene has important implications for reducing soil losses on N.
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spelling doaj-art-fa21a299d0a040cfa0d96b5204c8ca2f2025-07-25T13:15:16ZengMDPI AGBiology2079-77372025-07-0114787910.3390/biology14070879<i>Epichloë</i> Endophyte Alters Bacterial Nitrogen-Cycling Gene Abundance in the Rhizosphere Soil of Perennial RyegrassMunire Maimaitiyiming0Yanxiang Huang1Letian Jia2Mofan Wu3Zhenjiang Chen4Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Aairs, State Key Laboratory of Grassland Agro-Ecosystems, Engineering Research Center of Grassland Industry, Ministry of Education, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, ChinaKey Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Aairs, State Key Laboratory of Grassland Agro-Ecosystems, Engineering Research Center of Grassland Industry, Ministry of Education, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, ChinaKey Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Aairs, State Key Laboratory of Grassland Agro-Ecosystems, Engineering Research Center of Grassland Industry, Ministry of Education, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, ChinaKey Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Aairs, State Key Laboratory of Grassland Agro-Ecosystems, Engineering Research Center of Grassland Industry, Ministry of Education, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, ChinaKey Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Aairs, State Key Laboratory of Grassland Agro-Ecosystems, Engineering Research Center of Grassland Industry, Ministry of Education, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, ChinaPerennial ryegrass (<i data-eusoft-scrollable-element="1">Lolium perenne</i>), an important forage and turfgrass species, can establish a mutualistic symbiosis with the fungal endophyte <i data-eusoft-scrollable-element="1">Epichloë festucae</i> var. <i data-eusoft-scrollable-element="1">lolii.</i> Although the physiological and ecological impacts of endophyte infection on ryegrass have been extensively investigated, the response of the soil microbial community and nitrogen-cycling gene to this relationship has received much less attention. The present study emphasized abundance and diversity variation in the AOB-<i data-eusoft-scrollable-element="1">amoA</i>, <i data-eusoft-scrollable-element="1">nirK</i> and <i data-eusoft-scrollable-element="1">nosZ</i> functional genes in the rhizosphere soil of the endophyte–ryegrass symbiosis following litter addition. We sampled four times: at T<sub data-eusoft-scrollable-element="1">0</sub> (prior to first litter addition), T<sub data-eusoft-scrollable-element="1">1</sub> (post 120 d of 1st litter addition), T<sub data-eusoft-scrollable-element="1">2</sub> (post 120 d of 2nd litter addition) and T<sub data-eusoft-scrollable-element="1">3</sub> (post 120 d of 3rd litter addition) times. Real-time fluorescence quantitative PCR (qPCR) and PCR amplification and sequencing were used to characterize the abundance and diversity of the AOB-<i data-eusoft-scrollable-element="1">amoA</i>, <i data-eusoft-scrollable-element="1">nirK</i> and <i data-eusoft-scrollable-element="1">nosZ</i> genes in rhizosphere soils of endophyte-infected (E+) plants and endophyte-free (E−) plants. A significant enhancement of total Phosphorus (P), Soil Organic Carbon (SOC), Ammonium ion (NH<sub data-eusoft-scrollable-element="1">4</sub><sup data-eusoft-scrollable-element="1">+</sup>) and Nitrate ion (NO<sub data-eusoft-scrollable-element="1">3</sub><sup data-eusoft-scrollable-element="1">−</sup>) contents in the rhizosphere soil was recorded in endophyte-infected plants at different sampling times compared to endophyte-free plants (<i data-eusoft-scrollable-element="1">p</i> ≤ 0.05). The absolute abundance of the AOB-<i data-eusoft-scrollable-element="1">amoA</i> gene at T<sub data-eusoft-scrollable-element="1">0</sub> and T<sub data-eusoft-scrollable-element="1">1</sub> times was higher, as was the absolute abundance of the <i data-eusoft-scrollable-element="1">nosZ</i> gene at T<sub data-eusoft-scrollable-element="1">0</sub>, T<sub data-eusoft-scrollable-element="1">1</sub> and T<sub data-eusoft-scrollable-element="1">3</sub> times in the E+ plant rhizophere soils relative to E− plant rhizosphere soils. A significant change in relative abundance of the AOB-<i data-eusoft-scrollable-element="1">amoA</i> and <i data-eusoft-scrollable-element="1">nosZ</i> genes in the host rhizophere soils of endophyte-infected plants at T<sub data-eusoft-scrollable-element="1">1</sub> and T<sub data-eusoft-scrollable-element="1">3</sub> times was observed. The experiment failed to show any significant alteration in abundance and diversity of the <i data-eusoft-scrollable-element="1">nirK</i> gene, and diversity of the AOB-<i data-eusoft-scrollable-element="1">amoA</i> and <i data-eusoft-scrollable-element="1">nosZ</i> genes. Analysis of the abundance and diversity of the <i data-eusoft-scrollable-element="1">nirK</i> gene indicated that changes in soil properties accounted for approximately 70.38% of the variation along the first axis and 16.69% along the second axis, and soil NH<sub data-eusoft-scrollable-element="1">4</sub><sup data-eusoft-scrollable-element="1">+</sup> (<i data-eusoft-scrollable-element="1">p</i> = 0.002, 50.4%) and soil C/P ratio (<i data-eusoft-scrollable-element="1">p</i> = 0.012, 15.8%) had a strong effect. The changes in community abundance and diversity of the AOB-<i data-eusoft-scrollable-element="1">amoA</i> and <i data-eusoft-scrollable-element="1">nosZ</i> genes were mainly related to soil pH, N/P ratio and NH<sub data-eusoft-scrollable-element="1">4</sub><sup data-eusoft-scrollable-element="1">+</sup> content. The results demonstrate that the existence of tripartite interactions among the foliar endophyte <i data-eusoft-scrollable-element="1">E</i>. <i data-eusoft-scrollable-element="1">festucae</i> var. <i data-eusoft-scrollable-element="1">Lolii</i>, <i data-eusoft-scrollable-element="1">L. perenne</i> and soil nitrogen-cycling gene has important implications for reducing soil losses on N.https://www.mdpi.com/2079-7737/14/7/879<i>Epichloë endophyte</i><i>Lolium perenne</i>sampling timenitrogen-cycling geneabundance and diversity
spellingShingle Munire Maimaitiyiming
Yanxiang Huang
Letian Jia
Mofan Wu
Zhenjiang Chen
<i>Epichloë</i> Endophyte Alters Bacterial Nitrogen-Cycling Gene Abundance in the Rhizosphere Soil of Perennial Ryegrass
Biology
<i>Epichloë endophyte</i>
<i>Lolium perenne</i>
sampling time
nitrogen-cycling gene
abundance and diversity
title <i>Epichloë</i> Endophyte Alters Bacterial Nitrogen-Cycling Gene Abundance in the Rhizosphere Soil of Perennial Ryegrass
title_full <i>Epichloë</i> Endophyte Alters Bacterial Nitrogen-Cycling Gene Abundance in the Rhizosphere Soil of Perennial Ryegrass
title_fullStr <i>Epichloë</i> Endophyte Alters Bacterial Nitrogen-Cycling Gene Abundance in the Rhizosphere Soil of Perennial Ryegrass
title_full_unstemmed <i>Epichloë</i> Endophyte Alters Bacterial Nitrogen-Cycling Gene Abundance in the Rhizosphere Soil of Perennial Ryegrass
title_short <i>Epichloë</i> Endophyte Alters Bacterial Nitrogen-Cycling Gene Abundance in the Rhizosphere Soil of Perennial Ryegrass
title_sort i epichloe i endophyte alters bacterial nitrogen cycling gene abundance in the rhizosphere soil of perennial ryegrass
topic <i>Epichloë endophyte</i>
<i>Lolium perenne</i>
sampling time
nitrogen-cycling gene
abundance and diversity
url https://www.mdpi.com/2079-7737/14/7/879
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