Diversity and Functional Differences of Rhizosphere Microbial Communities in Maize Varieties with Different Resistance to Stalk Rot

doi:10.13560/j.cnki.biotech.bull.1985.2025-0999

Abstract

Abstract:

Objective This study aims to compare and analyze the structure, interaction networks, and functional profiles of the rhizosphere microbial communities in maize varieties with different resistances to stalk rot, to reveal their relationship with resistance to disease. Method We selected resistant (JK580, K2322) and susceptible (DK2207) varieties from 90 maize genotypes through field inoculation with the dominant pathogen Fusarium graminearum. Using 16S rRNA and ITS high-throughput sequencing, we then compared the diversity, composition, network structure, and functional potential of the rhizosphere microbiota in these varieties under pathogen stress. Result The α-diversity (Shannon and Pielou indexes) of the rhizosphere microbiome in the resistant maize varieties was significantly higher than that in the susceptible varieties. The β-diversity analysis showed that the bacterial and fungal community structures of the resistant varieties were more similar to each other and substantially different from those of the susceptible varieties. Composition and differential-taxa analyses revealed that the resistant varieties hosted a more diverse rhizosphere microbial community and were enriched with more beneficial taxa, such as Xanthomonadaceae, Microscillaceae, Oxalobacteraceae, and the fungal family Cladosporiaceae. In contrast, the susceptible variety DK2207 demonstrated a relatively simplistic community structure, primarily enriched with Pseudomonadaceae. Co-occurrence network analysis revealed that the rhizosphere microbial networks of the resistant varieties had higher robustness and lower vulnerability indices, indicating greater stability and resilience. Functional analysis further revealed that under pathogen stress, the rhizosphere bacteria of the resistant varieties maintained efficient energy acquisition functions, while the susceptible variety showed higher carbon and nitrogen metabolism and was enriched with more pathotrophic fungi. Conclusion Significant differences in the rhizosphere microbial community structure and function between resistant and susceptible maize varieties under pathogen stress. High microbial diversity, a greater variety of beneficial taxa and stable community networks may be important ecological mechanisms for enhancing stalk rot resistance in maize.

Key words: maize stalk rot, disease-resistant and susceptible varieties, rhizosphere microbial community, function prediction, high-throughput sequencing

PENG Shan-lin, LIAO Zhuo-cheng, WANG Tao, LIU Zhi-yu, LIU Hai-yi, WANG Ting-ting, YANG Qin, WANG Zhe, TAI Huan-huan. Diversity and Functional Differences of Rhizosphere Microbial Communities in Maize Varieties with Different Resistance to Stalk Rot[J]. Biotechnology Bulletin, 2026, 42(5): 1-13.

Figures/Tables 6

Fig. 1 Shannon indexes and Pielou indexes of rhizosphere bacterial (A, B) and fungal (C, D) communities of varieties with different resistance to maize stalk rot*P<0.05, **P<0.01; ***P<0.001, ****P<0.000 1. The ns refers to the non-significant effect (P>0.05); JK580、K2322 are maize varieties resistant to maize stalk rot, DK2207 is maize variety susceptible to maize stalk rot, The same as below

Fig. 2 Principal coordinate analysis of rhizosphere bacterial (A) and fungal (B) community (PCoA) of varieties with different resistance to maize stalk rot

Fig. 3 Composition of rhizosphere bacterial (A, B) and fungal (C, D) communities at phylum and family levels of varieties with different resistance to maize stalk rot

Fig. 4 LEfSe analysis of rhizosphere microbial biomarkers in maize varieties with different resistance to stalk rotA-B: The phylogenetic trees of the core biomarkers of bacterial (A) and fungal (B) biomarkers in rhizosphere microbial of the resistant variety K2322 and the susceptible variety DK2207 to maize stalk rot. C-D: The phylogenetic trees of the core biomarkers of bacterial (C) and fungal (D) biomarkers in rhizosphere microbial of the resistant variety JK580 and the susceptible variety DK2207 to maize stalk rot

Fig. 5 Bacterial and fungal co-occurrence network in rhizosphere microbial of varieties with different resistance to maize stalk rotA-C: Bacterial and fungal co-occurrence in rhizosphere of the susceptible variety DK2207 (A), and the resistant varieties JK580 (B), K2322 (C). D: Analysis of random removing of network nodes of the resistant and the susceptible varieties co-occurrence. E: Analysis of targeted removing of network nodes of the resistant and the susceptible varieties co-occurrence. F: Co-occurrence network vulnerability analysis of the resistant and the susceptible varieties. The nodes of each network are colored according to gate level classification, and the node size is determined according to the degree of connection. The edges in blue and red indicate co-occurrence and mutual exclusion patterns among taxa, respectively.

Fig. 6 Predictive functional analysis of rhizosphere (A) bacterial (FAPROTAX) and (B) fungal (FUNGuild) communities in maize varieties with different resistance to stalk rotDifferent lowercase letters in the figure indicate significant difference between different groups (P<0.05)

References 55

[1]	曾智勇. 我国玉米生产现状分析及建议 [J]. 粮油与饲料科技, 2022(3): 4-8.
	Zeng ZY. Analysis of the current situation of maize production in China and suggestions [J]. Grain Oil Feed Technol, 2022(3): 4-8.
[2]	范志业, 崔小伟, 施艳, 等. 河南省玉米茎基腐病主要病原菌鉴定及主栽玉米品种的抗性分析 [J]. 河南农业科学, 2014, 43(12): 87-90.
	Fan ZY, Cui XW, Shi Y, et al. Identification of pathogens causing corn stalk rot and resistance test of main cultivars in Henan Province [J]. J Henan Agric Sci, 2014, 43(12): 87-90.
[3]	马传禹, 姚丽姗, 杜腓利, 等. 玉米抗茎腐病研究进展 [J]. 玉米科学, 2018, 26(2): 131-137.
	Ma CY, Yao LS, Du FL, et al. Advanced resistance and genetic research for maize stalk rot [J]. J Maize Sci, 2018, 26(2): 131-137.
[4]	刘春来. 中国玉米茎腐病研究进展 [J]. 中国农学通报, 2017, 33(30): 130-134.
	Liu CL. Research process of maize stem rot in China [J]. Chin Agric Sci Bull, 2017, 33(30): 130-134.
[5]	Khokhar MK, Hooda KS, Sharma SS, et al. Post flowering stalk rot complex of maize - present status and future prospects [J]. Maydica, 2014, 59(3): 226-242.
[6]	段灿星, 曹言勇, 董怀玉, 等. 玉米种质资源抗腐霉茎腐病和镰孢茎腐病精准鉴定 [J]. 中国农业科学, 2022, 55(2): 265-279.
	Duan CX, Cao YY, Dong HY, et al. Precise characterization of maize germplasm for resistance to Pythium stalk rot and Gibberella stalk rot [J]. Sci Agric Sin, 2022, 55(2): 265-279.
[7]	马海林, 刘峰, 崔贵梅, 等. 不同种衣剂配方防治玉米茎腐病效果试验 [J]. 陕西农业科学, 2020, 66(7): 28-31, 57.
	Ma HL, Liu F, Cui GM, et al. Experiment on effect of different seed coating formulas on control of maize stem rot [J]. Shaanxi J Agric Sci, 2020, 66(7): 28-31, 57.
[8]	李想, 王欢欢, 郭秋翠, 等. 玉米茎腐病病原禾谷镰孢拮抗菌筛选及分子鉴定 [J]. 玉米科学, 2020, 28(5): 169-175.
	Li X, Wang HH, Guo QC, et al. Isolation and molecular identification of antagonistic bacteria against the pathogen Fusarium graminearum causing corn stalk rot [J]. J Maize Sci, 2020, 28(5): 169-175.
[9]	韦中, 沈宗专, 杨天杰, 等. 从抑病土壤到根际免疫: 概念提出与发展思考 [J]. 土壤学报, 2021, 58(4): 814-824.
	Wei Z, Shen ZZ, Yang TJ, et al. From suppressive soil to rhizosphere immunity: towards an ecosystem thinking for soil-borne pathogen control [J]. Acta Pedol Sin, 2021, 58(4): 814-824.
[10]	Berendsen RL, Vismans G, Yu K, et al. Disease-induced assemblage of a plant-beneficial bacterial consortium [J]. ISME J, 2018, 12(6): 1496-1507.
[11]	Philippot L, Raaijmakers JM, Lemanceau P, et al. Going back to the roots: the microbial ecology of the rhizosphere [J]. Nat Rev Microbiol, 2013, 11(11): 789-799.
[12]	李金鞠, 廖甜甜, 潘虹, 等. 土壤有益微生物在植物病害防治中的应用 [J]. 湖北农业科学, 2011, 50(23): 4753-4757.
	Li JJ, Liao TT, Pan H, et al. Application of beneficial soil microorganisms in biological control of crop diseases [J]. Hubei Agric Sci, 2011, 50(23): 4753-4757.
[13]	荀卫兵, 张瑞福, 沈其荣. 根际微生物组功能补偿装配的概念、内涵和展望 [J]. 土壤学报, 2024, 61(6): 1481-1491.
	Xun WB, Zhang RF, Shen QR. Functional compensatory assembly of rhizosphere microbiome: concept, content, and outlook [J]. Acta Pedol Sin, 2024, 61(6): 1481-1491.
[14]	Yang KM, Fu RX, Feng HC, et al. RIN enhances plant disease resistance via root exudate-mediated assembly of disease-suppressive rhizosphere microbiota [J]. Mol Plant, 2023, 16(9): 1379-1395.
[15]	Mendes LW, Mendes R, Raaijmakers JM, et al. Breeding for soil-borne pathogen resistance impacts active rhizosphere microbiome of common bean [J]. ISME J, 2018, 12(12): 3038-3042.
[16]	高小宁, 刘睿, 吴自林, 等. 宿根矮化病抗感甘蔗品种茎部内生真菌和细菌群落特征分析 [J]. 生物技术通报, 2022, 38(6): 166-173.
	Gao XN, Liu R, Wu ZL, et al. Characteristics of endophytic fungal and bacterial community in the stalks of sugarcane cultivars resistant to ratoon stunting disease [J]. Biotechnol Bull, 2022, 38(6): 166-173.
[17]	Jin X, Jia HT, Ran LY, et al. Fusaric acid mediates the assembly of disease-suppressive rhizosphere microbiota via induced shifts in plant root exudates [J]. Nat Commun, 2024, 15: 5125.
[18]	Ping XX, Khan RAA, Chen SM, et al. Deciphering the role of rhizosphere microbiota in modulating disease resistance in cabbage varieties [J]. Microbiome, 2024, 12(1): 160.
[19]	Yin JK, Zhang ZL, Zhu CC, et al. Heritability of tomato rhizobacteria resistant to Ralstonia solanacearum [J]. Microbiome, 2022, 10(1): 227.
[20]	Ge AH, Liang ZH, Xiao JL, et al. Microbial assembly and association network in watermelon rhizosphere after soil fumigation for Fusarium wilt control [J]. Agric Ecosyst Environ, 2021, 312: 107336.
[21]	李红, 晋齐鸣, 张伟, 等. 玉米品种抗茎腐病鉴定 [J]. 东北农业科学, 2017, 42(2): 32-33.
	Li H, Jin QM, Zhang W, et al. Identification of resistance to stalk rot of maize varieties [J]. J Northeast Agric Sci, 2017, 42(2): 32-33.
[22]	Xia XY, Wei QH, Wu HX, et al. Bacillus species are core microbiota of resistant maize cultivars that induce host metabolic defense against corn stalk rot [J]. Microbiome, 2024, 12(1): 156.
[23]	Epelde L, Becerril JM, Hernández-Allica J, et al. Functional diversity as indicator of the recovery of soil health derived from Thlaspi caerulescens growth and metal phytoextraction [J]. Appl Soil Ecol, 2008, 39(3): 299-310.
[24]	Callahan BJ, McMurdie PJ, Rosen MJ, et al. DADA2: High-resolution sample inference from Illumina amplicon data [J]. Nat Meth, 2016, 13(7): 581-583.
[25]	Pruesse E, Quast C, Knittel K, et al. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB [J]. Nucleic Acids Res, 2007, 35(21): 7188-7196.
[26]	Kõljalg U, Larsson KH, Abarenkov K, et al. UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi [J]. New Phytol, 2005, 166(3): 1063-1068.
[27]	Lyu FY, Han FR, Ge CL, et al. OmicStudio: a composable bioinformatics cloud platform with real-time feedback that can generate high-quality graphs for publication [J]. iMeta, 2023, 2(1): e85.
[28]	Nguyen NH, Song ZW, Bates ST, et al. FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild [J]. Fungal Ecol, 2016, 20: 241-248.
[29]	Gao YY, Zhang GX, Jiang SY, et al. Wekemo Bioincloud: a user-friendly platform for meta-omics data analyses [J]. iMeta, 2024, 3(1): e175.
[30]	Yue H, Sun XM, Wang TT, et al. Host genotype-specific rhizosphere fungus enhances drought resistance in wheat [J]. Microbiome, 2024, 12(1): 44.
[31]	Dlamini SP, Akanmu AO, Babalola OO. Rhizospheric microorganisms: The gateway to a sustainable plant health [J]. Front Sustain Food Syst, 2022, 6: 925802.
[32]	石博, 谢媛媛, 关峰, 等. 苦瓜枯萎病抗病与感病品种根际土壤的微生物数量消长动态分析 [J]. 中国农学通报, 2024, 40(22): 118-124.
	Shi B, Xie YY, Guan F, et al. Analysis on population fluctuation of rhizosphere microorganism of resistant and susceptible bitter gourd [J]. Chin Agric Sci Bull, 2024, 40(22): 118-124.
[33]	Wei Z, Yang TJ, Friman VP, et al. Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health [J]. Nat Commun, 2015, 6: 8413.
[34]	Venturi V, Keel C. Signaling in the rhizosphere [J]. Trends Plant Sci, 2016, 21(3): 187-198.
[35]	Caporaso JG, Lauber CL, Walters WA, et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample [J]. Proc Natl Acad Sci U S A, 2011, 108(supplement_1): 4516-4522.
[36]	Feng ZW, Liang QH, Yao Q, et al. The role of the rhizobiome recruited by root exudates in plant disease resistance: current status and future directions [J]. Environ Microbiome, 2024, 19(1): 91.
[37]	姜淑祯, 冯小虎, 宋文静, 等. 不同青枯病抗性烤烟品种(系)根际土壤微生物群落分析 [J]. 烟草科技, 2025, 58(4): 34-44.
	Jiang SZ, Feng XH, Song WJ, et al. Analysis of microbial communities in rhizosphere soil for flue-cured tobacco varieties(lines) with different resistance to bacterial wilt [J]. Tob Sci Technol, 2025, 58(4): 34-44.
[38]	Shao MW, Chen HJ, Huang AQ, et al. Modulation of rhizosphere microbiota by Bacillus subtilis R31 enhances long-term suppression of banana Fusarium wilt [J]. iMetaOmics, 2025, 2(2): e70006.
[39]	Deng XH, Zhang N, Li YC, et al. Bio-organic soil amendment promotes the suppression of Ralstonia solanacearum by inducing changes in the functionality and composition of rhizosphere bacterial communities [J]. New Phytol, 2022, 235(4): 1558-1574.
[40]	Wang DN, He XM, Baer M, et al. Lateral root enriched Massilia associated with plant flowering in maize [J]. Microbiome, 2024, 12(1): 124.
[41]	Yu P, He XM, Baer M, et al. Plant flavones enrich rhizosphere Oxalobacteraceae to improve maize performance under nitrogen deprivation [J]. Nat Plants, 2021, 7(4): 481-499.
[42]	Wang XN, Radwan MM, Taráwneh AH, et al. Antifungal activity against plant pathogens of metabolites from the endophytic fungus Cladosporium cladosporioides [J]. J Agric Food Chem, 2013, 61(19): 4551-4555.
[43]	Fan XY, Ge AH, Qi SS, et al. Root exudates and microbial metabolites: signals and nutrients in plant-microbe interactions [J]. Sci China Life Sci, 2025, 68(8): 2290-2302.
[44]	He DX, Singh SK, Peng L, et al. Flavonoid-attracted Aeromonas sp. from the Arabidopsis root microbiome enhances plant dehydration resistance [J]. ISME J, 2022, 16(11): 2622-2632.
[45]	Thimmaraju Rudrappa KJC. Root-secreted malic acid recruits beneficial soil bacteria[J]. Plant Physiol, 2008, 148(3): 1547-1556.
[46]	Li PF, Liu J, Saleem M, et al. Reduced chemodiversity suppresses rhizosphere microbiome functioning in the mono-cropped agroecosystems [J]. Microbiome, 2022, 10(1): 108.
[47]	Wang CQ, Kuzyakov Y. Mechanisms and implications of bacterial-fungal competition for soil resources [J]. ISME J, 2024, 18(1): wrae073.
[48]	程玉静, 陈国清, 薛林, 等. 玉米茎腐病研究进展 [J]. 安徽农业科学, 2013, 41(20): 8557-8559.
	Cheng YJ, Chen GQ, Xue L, et al. Research advance of maize stalk rot [J]. J Anhui Agric Sci, 2013,41(20): 8557-8559.
[49]	赵同谦, 张凯, 郑华, 等. 外来植物对陆地生态系统氮循环的影响途径 [J]. 生态科学, 2011, 30(2): 207-212.
	Zhao TQ, Zhang K, Zheng H, et al. Pathways of exotic plant impacts on nitrogen cycling in terrestrial ecosystem [J]. Ecol Sci, 2011, 30(2): 207-212.
[50]	Wang SC, Zhang XY, Zhang ZC, et al. Fusarium-produced vitamin B6 promotes the evasion of soybean resistance by Phytophthora sojae [J]. J Integr Plant Biol, 2023, 65(9): 2204-2217.
[51]	Thébault E, Fontaine C. Stability of ecological communities and the architecture of mutualistic and trophic networks [J]. Science, 2010, 329(5993): 853-856.
[52]	Rohr RP, Saavedra S, Bascompte J. On the structural stability of mutualistic systems [J]. Science, 2014, 345(6195): 1253497.
[53]	Wu CF, Liu HW, Lai LY, et al. Host genotype-specific plant microbiome correlates with wheat disease resistance [J]. Biol Fertil Soils, 2025, 61(2): 277-291.
[54]	Fang TY, Han XY, Yue YL. Disease-resistant varieties of Chinese cabbage (Brassica rapa L. ssp. pekinensis) inhibit Plasmodiophora brassicae infestation by stabilising root flora structure [J]. Front Plant Sci, 2024, 15: 1328845.
[55]	Qiao YZ, Wang TT, Huang QW, et al. Core species impact plant health by enhancing soil microbial cooperation and network complexity during community coalescence [J]. Soil Biol Biochem, 2024, 188: 109231.