Dictyophora indusiata and Bacillus aryabhattai improve sugarcane yield by endogenously associating with the root and regulating flavonoid metabolism

IntroductionEndophytes play a significant role in regulating plant root development and facilitating nutrient solubilization and transportation. This association could improve plant growth. The present study has uncovered a distinct phenotype, which we refer to as "white root", arising fro...

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Main Authors: Mingzheng Duan, Xiang Li, Xiaojian Wu, Shengfeng Long, Hairong Huang, Yijie Li, Qi-Huai Liu, Guanghu Zhu, Bin Feng, Sunqian Qin, Changning Li, Hai Yang, Jie Qin, Zhendong Chen, Zeping Wang
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-03-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2024.1326917/full
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author Mingzheng Duan
Mingzheng Duan
Xiang Li
Xiaojian Wu
Shengfeng Long
Hairong Huang
Yijie Li
Qi-Huai Liu
Guanghu Zhu
Bin Feng
Sunqian Qin
Changning Li
Hai Yang
Jie Qin
Zhendong Chen
Zeping Wang
author_facet Mingzheng Duan
Mingzheng Duan
Xiang Li
Xiaojian Wu
Shengfeng Long
Hairong Huang
Yijie Li
Qi-Huai Liu
Guanghu Zhu
Bin Feng
Sunqian Qin
Changning Li
Hai Yang
Jie Qin
Zhendong Chen
Zeping Wang
author_sort Mingzheng Duan
collection DOAJ
description IntroductionEndophytes play a significant role in regulating plant root development and facilitating nutrient solubilization and transportation. This association could improve plant growth. The present study has uncovered a distinct phenotype, which we refer to as "white root", arising from the intricate interactions between endophytic fungi and bacteria with the roots in a sugarcane and bamboo fungus (Dictyophora indusiata) intercropping system.MethodsWe investigated the mechanisms underlying the formation of this “white root” phenotype and its impact on sugarcane yield and metabolism by metabarcoding and metabolome analysis.Results and DiscussionInitial analysis revealed that intercropping with D. indusiata increased sugarcane yield by enhancing the number of viable tillers compared with bagasse and no input control. Metabarcoding based on second-generation and third-generation sequencing indicated that D. indusiate and Bacillus aryabhattai dominates the fungal and bacterial composition in the “white root” phenotype of sugarcane root. The coexistence of D. indusiata and B. aryabhattai as endophytes induced plant growth-promoting metabolites in the sugarcane root system, such as lysoPC 18:1 and dihydrobenzofuran, probably contributing to increased sugarcane yield. Furthermore, the association also enhanced the metabolism of compounds, such as naringenin-7-O-glucoside (Prunin), naringenin-7-O-neohesperidoside (Naringin)*, hesperetin-7-O-neohesperidoside (Neohesperidin), epicatechin, and aromadendrin (Dihydrokaempferol), involved in flavonoid metabolism during the formation of the endophytic phenotype in the sugarcane root system. These observations suggest that the “white root” phenotype promotes sugarcane growth by activating flavonoid metabolism. This study reports an interesting phenomenon where D. indusiata, coordinate with the specific bacteria invade, forms a “white root” phenotype with sugarcane root. The study also provides new insights into using D. indusiata as a soil inoculant for promoting sugarcane growth and proposes a new approach for improve sugarcane cultivation.
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spelling doaj.art-9791ed46afed40e5acac043a6269058d2024-03-07T05:03:40ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2024-03-011510.3389/fpls.2024.13269171326917Dictyophora indusiata and Bacillus aryabhattai improve sugarcane yield by endogenously associating with the root and regulating flavonoid metabolismMingzheng Duan0Mingzheng Duan1Xiang Li2Xiaojian Wu3Shengfeng Long4Hairong Huang5Yijie Li6Qi-Huai Liu7Guanghu Zhu8Bin Feng9Sunqian Qin10Changning Li11Hai Yang12Jie Qin13Zhendong Chen14Zeping Wang15Guangxi Academy of Agricultural Sciences, Nanning, ChinaYunnan Key Laboratory of Gastrodia Elata and Fungal Symbiotic Biology, College of Agronomy and Life Sciences, Zhaotong University, Zhaotong, ChinaGuangxi Academy of Agricultural Sciences, Nanning, ChinaGuangxi Academy of Agricultural Sciences, Nanning, ChinaGuangxi Academy of Agricultural Sciences, Nanning, ChinaGuangxi Academy of Agricultural Sciences, Nanning, ChinaGuangxi Academy of Agricultural Sciences, Nanning, ChinaLaibin Academy of Agricultural Sciences, Laibin, ChinaLaibin Academy of Agricultural Sciences, Laibin, ChinaLaibin Academy of Agricultural Sciences, Laibin, ChinaLaibin Academy of Agricultural Sciences, Laibin, ChinaGuangxi Academy of Agricultural Sciences, Nanning, ChinaGuangxi Academy of Agricultural Sciences, Nanning, ChinaGuangxi Academy of Agricultural Sciences, Nanning, ChinaGuangxi Academy of Agricultural Sciences, Nanning, ChinaGuangxi Academy of Agricultural Sciences, Nanning, ChinaIntroductionEndophytes play a significant role in regulating plant root development and facilitating nutrient solubilization and transportation. This association could improve plant growth. The present study has uncovered a distinct phenotype, which we refer to as "white root", arising from the intricate interactions between endophytic fungi and bacteria with the roots in a sugarcane and bamboo fungus (Dictyophora indusiata) intercropping system.MethodsWe investigated the mechanisms underlying the formation of this “white root” phenotype and its impact on sugarcane yield and metabolism by metabarcoding and metabolome analysis.Results and DiscussionInitial analysis revealed that intercropping with D. indusiata increased sugarcane yield by enhancing the number of viable tillers compared with bagasse and no input control. Metabarcoding based on second-generation and third-generation sequencing indicated that D. indusiate and Bacillus aryabhattai dominates the fungal and bacterial composition in the “white root” phenotype of sugarcane root. The coexistence of D. indusiata and B. aryabhattai as endophytes induced plant growth-promoting metabolites in the sugarcane root system, such as lysoPC 18:1 and dihydrobenzofuran, probably contributing to increased sugarcane yield. Furthermore, the association also enhanced the metabolism of compounds, such as naringenin-7-O-glucoside (Prunin), naringenin-7-O-neohesperidoside (Naringin)*, hesperetin-7-O-neohesperidoside (Neohesperidin), epicatechin, and aromadendrin (Dihydrokaempferol), involved in flavonoid metabolism during the formation of the endophytic phenotype in the sugarcane root system. These observations suggest that the “white root” phenotype promotes sugarcane growth by activating flavonoid metabolism. This study reports an interesting phenomenon where D. indusiata, coordinate with the specific bacteria invade, forms a “white root” phenotype with sugarcane root. The study also provides new insights into using D. indusiata as a soil inoculant for promoting sugarcane growth and proposes a new approach for improve sugarcane cultivation.https://www.frontiersin.org/articles/10.3389/fpls.2024.1326917/fullBacillusfull-length 16S rRNAmetabolomemetabarcodingplant growthsugarcane root
spellingShingle Mingzheng Duan
Mingzheng Duan
Xiang Li
Xiaojian Wu
Shengfeng Long
Hairong Huang
Yijie Li
Qi-Huai Liu
Guanghu Zhu
Bin Feng
Sunqian Qin
Changning Li
Hai Yang
Jie Qin
Zhendong Chen
Zeping Wang
Dictyophora indusiata and Bacillus aryabhattai improve sugarcane yield by endogenously associating with the root and regulating flavonoid metabolism
Frontiers in Plant Science
Bacillus
full-length 16S rRNA
metabolome
metabarcoding
plant growth
sugarcane root
title Dictyophora indusiata and Bacillus aryabhattai improve sugarcane yield by endogenously associating with the root and regulating flavonoid metabolism
title_full Dictyophora indusiata and Bacillus aryabhattai improve sugarcane yield by endogenously associating with the root and regulating flavonoid metabolism
title_fullStr Dictyophora indusiata and Bacillus aryabhattai improve sugarcane yield by endogenously associating with the root and regulating flavonoid metabolism
title_full_unstemmed Dictyophora indusiata and Bacillus aryabhattai improve sugarcane yield by endogenously associating with the root and regulating flavonoid metabolism
title_short Dictyophora indusiata and Bacillus aryabhattai improve sugarcane yield by endogenously associating with the root and regulating flavonoid metabolism
title_sort dictyophora indusiata and bacillus aryabhattai improve sugarcane yield by endogenously associating with the root and regulating flavonoid metabolism
topic Bacillus
full-length 16S rRNA
metabolome
metabarcoding
plant growth
sugarcane root
url https://www.frontiersin.org/articles/10.3389/fpls.2024.1326917/full
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