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Article(id=1226460581994086907, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1226460576751206672, articleNumber=null, orderNo=null, doi=10.13343/j.cnki.wsxb.20250039, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1736870400000, receivedDateStr=2025-01-15, revisedDate=null, revisedDateStr=null, acceptedDate=1742486400000, acceptedDateStr=2025-03-21, onlineDate=1770340589283, onlineDateStr=2026-02-06, pubDate=1754236800000, pubDateStr=2025-08-04, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1770340589283, onlineIssueDateStr=2026-02-06, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1770340589283, creator=13701087609, updateTime=1770340589283, updator=13701087609, issue=Issue{id=1226460576751206672, tenantId=1146029695717560320, journalId=1192105938417971205, year='2025', volume='65', issue='8', pageStart='1', pageEnd='3812', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1770340588033, creator=13701087609, updateTime=1770363610188, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1226557138735117113, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1226460576751206672, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1226557138735117114, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1226460576751206672, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=3600, endPage=3614, ext={EN=ArticleExt(id=1226460582866502233, articleId=1226460581994086907, tenantId=1146029695717560320, journalId=1192105938417971205, language=EN, title=Phyllosphere microbial community structure and diversity of Areca catechu with yellow leaf disease, columnId=1192149543992045670, journalTitle=Acta Microbiologica Sinica, columnName=Research Article, runingTitle=null, highlight=null, articleAbstract=

[Objective] To clarify phyllosphere microbial responses to the invasion of areca palm velarivirus 1 (APV1), a virus causing yellow leaf disease of areca (Areca catechu), and provide a theoretical basis and technical support for the study of phyllosphere micro-ecology, exploration of excellent biocontrol resources, and green prevention and control of yellow leaf disease of areca. [Methods] We collected healthy leaves, mildly diseased leaves, and severely diseased leaves of areca. The phyllosphere microbial community structure and diversity were compared by high-throughput sequencing and bioinformatics methods. Furthermore, functional differences of phyllosphere microbial communities were analyzed. [Results] The dominant bacterial phyla in the phyllosphere of areca included Actinobacteriota, Proteobacteria, Acidobacteriota, Firmicutes, and Myxococcota, while the dominant fungal phyla were Ascomycota and Basidiomycota. As the disease became increasingly severe, bacterial richness initially increased then decreased while fungal richness initially decreased then increased. However, both bacterial diversity and fungal diversity showed a trend of first increasing and then decreasing. Firmicutes and Basidiomycota served as indicators of mildly diseased areca, with the relative abundance showing consistent trends with alpha diversity. The healthy plants and the diseased plants showed different phyllosphere microbial functions. Specifically, the environmental information processing function was significantly higher in severely diseased areca plants than in healthy ones. Additionally, the relative abundance of symbiotroph fungi in the phyllosphere were significantly higher in severely diseased areca plants than in healthy ones. [Conclusion] The yellow leaf disease significantly alters the phyllosphere microbial community structure and diversity of areca, with greater changes during the early disease stage. This suggests that areca may defend against APV1 infection by recruiting beneficial microorganisms, regulating cellular metabolism and biochemical reactions, and activating autoimmunity.

, correspAuthors=Kai RUI, authorNote=null, correspAuthorsNote=
*E-mail:
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【目的】 明确叶际微生物对槟榔黄化病APV1病毒入侵的响应，为槟榔叶际微生态的研究、优异生防资源的挖掘及槟榔黄化病的绿色防控提供理论依据和技术支持。 【方法】 分别采集健康、轻度发病及重度发病槟榔叶片，通过高通量测序技术和生物信息学方法比较叶际微生物的群落结构与多样性并分析功能差异。 【结果】 槟榔叶际优势细菌门为放线菌门(Actinobacteriota)、变形菌门(Proteobacteria)、酸杆菌门(Acidobacteriota)、厚壁菌门(Firmicutes)和黏球菌门(Myxococcota)，优势真菌门为子囊菌门(Ascomycota)和担子菌门(Basidiomycota)。随着发病程度的增加，槟榔叶际细菌丰富度先升后降，真菌丰富度先降后升；细菌和真菌多样性均呈先升后降的趋势。厚壁菌门(Firmicutes)和担子菌门(Basidiomycota)作为轻度发病槟榔的标志物种，其相对丰度与α多样性变化趋势一致。健康与不同发病程度槟榔叶际微生物功能均发生了不同程度的变化，其中重度发病槟榔的环境信息处理功能显著高于健康槟榔；共生营养型(symbiotroph)的相对丰度极显著高于健康槟榔。 【结论】 槟榔黄化病显著改变了叶际微生物群落结构与多样性，且在发病初期变化较大，说明槟榔可能通过招募有益微生物、调控细胞代谢、生化反应、进行自身免疫等方式来抵御APV1病毒侵染。

, correspAuthors=芮凯, authorNote=null, correspAuthorsNote=null, copyrightStatement=null, copyrightOwner=null, extLink=null, articleAbsUrl=null, sourceXml=2FnT+tKz9FpreZGPhVoMKg==, magXml=PoaY5oLlnRU1zuZFr38+gQ==, pdfUrl=null, pdf=73IUaXjG2UyWgUCiTzCaCw==, pdfFileSize=2303800, pdfExtLink=null, richHtmlUrl=null, mobilePdfUrl=null, reviewReport=null, pdfFirstPage=null, abstractGraph=4M9UJm5ELmyPqxeAnBJIRg==, abstractGraphContent=null, abstractVideo=null, citation=null, cebUrl=null, magXmlContent=XNeYXXv8m8DHG8HiQDL/Rw==, mapNumber=null, authorCompany=null, fund=null, authors=

作者贡献声明

马瑞：数据分析与可视化呈现、论文撰写和修改；王贞霖：样品采集与实验操作、数据收集和处理、写作初稿与修改；芮凯：调查研究、提供资源、指导。

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A: Bacterial community; B: Fungal community., figureFileSmall=f4lPCuHpMFl9RvFnq+3DPA==, figureFileBig=KbykCETrBrwMAn+rveSsYQ==, tableContent=null), ArticleFig(id=1226596296719512398, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460581994086907, language=CN, label=图1, caption=稀释曲线。A：细菌群落；B：真菌群落。, figureFileSmall=f4lPCuHpMFl9RvFnq+3DPA==, figureFileBig=KbykCETrBrwMAn+rveSsYQ==, tableContent=null), ArticleFig(id=1226596296857924447, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460581994086907, language=EN, label=Figure 2, caption=Venn of ASVs level. A: Bacterial community; B: Fungal community., figureFileSmall=yhCxX9Rka/sJ66aphqKxpQ==, figureFileBig=hgJfvS1K2wX+5Hm0RLOvhQ==, tableContent=null), ArticleFig(id=1226596296946004840, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460581994086907, language=CN, label=图2, caption=ASV水平下venn图。A：细菌群落；B：真菌群落。, figureFileSmall=yhCxX9Rka/sJ66aphqKxpQ==, figureFileBig=hgJfvS1K2wX+5Hm0RLOvhQ==, tableContent=null), ArticleFig(id=1226596297046668146, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460581994086907, language=EN, label=Figure 3, caption=Areca phyllosphere microbial relative abundance at phylum level. A: Bacterial community; B: Fungal community., figureFileSmall=CXpnqzzv4CwOZk+UJIsOfA==, figureFileBig=0EsoaNon/pW+yDJd6GU1IQ==, tableContent=null), ArticleFig(id=1226596297172497285, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460581994086907, language=CN, label=图3, caption=槟榔叶际物种相对丰度图(门水平)。A：细菌群落；B：真菌群落。, figureFileSmall=CXpnqzzv4CwOZk+UJIsOfA==, figureFileBig=0EsoaNon/pW+yDJd6GU1IQ==, tableContent=null), ArticleFig(id=1226596297306715027, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460581994086907, language=EN, label=Figure 4, caption=Areca phyllosphere microbial relative abundance at genus level. A: Bacterial community; B: Fungal community., figureFileSmall=q3yzsliq0tcx0kh13DfzBw==, figureFileBig=JP1vIpzMx9Kw13yl7+VIxQ==, tableContent=null), ArticleFig(id=1226596297428349858, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460581994086907, language=CN, label=图4, caption=槟榔叶际物种相对丰度图(属水平)。A：细菌群落；B：真菌群落。, figureFileSmall=q3yzsliq0tcx0kh13DfzBw==, figureFileBig=JP1vIpzMx9Kw13yl7+VIxQ==, tableContent=null), ArticleFig(id=1226596297537401774, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460581994086907, language=EN, label=Figure 5, caption=Alpha diversity index comparison of areca phyllosphere microbial community. A: Chao1 index of bacterial community; B: Shannon index of bacterial community; C: Chao1 index of fungal community; D:Shannon index of fungal community. * and ** respectively represent significant (P<0.05) and extremely significant (P<0.01) levels of correlation., figureFileSmall=Xlxe/5ulrHOBge3BdOpmCw==, figureFileBig=0CZgfZCxwvmFoBMLjuB00Q==, tableContent=null), ArticleFig(id=1226596297642259382, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460581994086907, language=CN, label=图5, caption=槟榔叶际微生物群落的α多样性指数比较。A：细菌群落Chao1指数；B：细菌群落Shannon指数；C：真菌群落Chao1指数；D：真菌群落Shannon指数。*与**分别代表相关性达到显著(P<0.05)和极显著水平(P<0.01)。, figureFileSmall=Xlxe/5ulrHOBge3BdOpmCw==, figureFileBig=0CZgfZCxwvmFoBMLjuB00Q==, tableContent=null), ArticleFig(id=1226596297784865733, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460581994086907, language=EN, label=Figure 6, caption=Principal coordinates analysis based on Bray-Curtis algorithm. A: Bacterial community; B: Fungal community., figureFileSmall=/MN4hGvbU4HCYqiRkprD7w==, figureFileBig=hcmRWkMNbIiNeuSmAJXSzg==, tableContent=null), ArticleFig(id=1226596297910694865, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460581994086907, language=CN, label=图6, caption=基于Bray-Curtis算法的主坐标分析(PCoA)。A：细菌群落；B：真菌群落。, figureFileSmall=/MN4hGvbU4HCYqiRkprD7w==, figureFileBig=hcmRWkMNbIiNeuSmAJXSzg==, tableContent=null), ArticleFig(id=1226596298061689821, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460581994086907, language=EN, label=Figure 7, caption=UPGMA clustering analysis. A: Bacterial community; B: Fungal community., figureFileSmall=/ZMqA0zgQ1d5Rp05Po/F9g==, figureFileBig=2jfbMZPlS3rOJ+vJrqSpew==, tableContent=null), ArticleFig(id=1226596298204296169, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460581994086907, language=CN, label=图7, caption=UPGMA聚类分析。A：细菌群落；B：真菌群落。, figureFileSmall=/ZMqA0zgQ1d5Rp05Po/F9g==, figureFileBig=2jfbMZPlS3rOJ+vJrqSpew==, tableContent=null), ArticleFig(id=1226596298342708216, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460581994086907, language=EN, label=Figure 8, caption=LEfSe analysis of areca phyllosphere bacterial community (LDA>4)., figureFileSmall=52fwTTKcoKivkK/hRSydhQ==, figureFileBig=UwKrr+tdSzgjmMMOk55YCQ==, tableContent=null), ArticleFig(id=1226596299705857023, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460581994086907, language=CN, label=图8, caption=槟榔叶际细菌群落LEfSe分析(LDA>4), figureFileSmall=52fwTTKcoKivkK/hRSydhQ==, figureFileBig=UwKrr+tdSzgjmMMOk55YCQ==, tableContent=null), ArticleFig(id=1226596299890405390, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460581994086907, language=EN, label=Figure 9, caption=LEfSe analysis of areca phyllosphere fungal community (LDA>3.5)., figureFileSmall=TOeauieqawF2zqwCuoFS6A==, figureFileBig=d/vUN8LjweATUksouDE5+A==, tableContent=null), ArticleFig(id=1226596300037206039, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460581994086907, language=CN, label=图9, caption=槟榔叶际真菌群落LEfSe分析(LDA>3.5), figureFileSmall=TOeauieqawF2zqwCuoFS6A==, figureFileBig=d/vUN8LjweATUksouDE5+A==, tableContent=null), ArticleFig(id=1226596300154646564, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460581994086907, language=EN, label=Figure 10, caption=KEGG primary functional prediction of areca phyllosphere bacteria. A: Primary functional composition; B: Primary functional differences (SD vs. JK)., figureFileSmall=+csKCBIuv336GtEqoU1eDw==, figureFileBig=AYRGbnTMPOFs14uvvcJ7ug==, tableContent=null), ArticleFig(id=1226596300272087084, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460581994086907, language=CN, label=图10, caption=槟榔叶际细菌的KEGG一级功能预测。A：一级功能组成；B：一级功能差异(SD和JK)。, figureFileSmall=+csKCBIuv336GtEqoU1eDw==, figureFileBig=AYRGbnTMPOFs14uvvcJ7ug==, tableContent=null), ArticleFig(id=1226596300397916211, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460581994086907, language=EN, label=Figure 11, caption=KEGG secondary functional prediction of areca phyllosphere bacteria. A: Secondary functional composition; B: Secondary functional differences (SD vs. JK); C: Secondary functional differences (SD vs. MD)., figureFileSmall=NEt6RM6USi4/ViEP/5mHOg==, figureFileBig=XR496/pVYTO+jzpvdAE4Mw==, tableContent=null), ArticleFig(id=1226596300536328252, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460581994086907, language=CN, label=图11, caption=槟榔叶际细菌的KEGG二级功能预测。A：二级功能组成；B：二级功能差异(SD和JK)；C：二级功能差异(SD和MD)。, figureFileSmall=NEt6RM6USi4/ViEP/5mHOg==, figureFileBig=XR496/pVYTO+jzpvdAE4Mw==, tableContent=null), ArticleFig(id=1226596300666351683, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460581994086907, language=EN, label=Figure 12, caption=Functional prediction of areca phyllosphere fungus. 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槟榔黄化病叶际微生物群落结构与多样性
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马瑞 1 , 王贞霖 1 , 芮凯 2, *
微生物学报 | 研究报告 2025,65(8): 3600-3614
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微生物学报 | 研究报告 2025, 65(8): 3600-3614
槟榔黄化病叶际微生物群落结构与多样性
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马瑞1, 王贞霖1, 芮凯2, *
作者信息
  • 1.海南省农业科学院植物保护研究所，海南省农业科学院农产品质量安全与标准研究中心，海南省植物病虫害防控重点实验室，农业农村部海口作物有害生物科学观测实验站，海南 海口
  • 2.海南省农业科学院三亚研究院，海南 三亚
Phyllosphere microbial community structure and diversity of Areca catechu with yellow leaf disease
Rui MA1, Zhenlin WANG1, Kai RUI2, *
Affiliations
  • 1.Scientific Observation and Experiment Station of Crop Pests in Haikou Ministry of Agriculture, Key Laboratory of Plant Diseases and Pest Control of Hainan Province, Sciences Research Center of Quality Safety and Standards for Agricultural Products of Hainan Academy of Agricultural Sciences, Institute of Plant Protection, Hainan Academy of Agricultural Sciences, Haikou, Hainan, China
  • 2.Sanya Institute of Hainan Academy of Agricultural Sciences, Sanya, Hainan, China
出版时间: 2025-08-04 doi: 10.13343/j.cnki.wsxb.20250039
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【目的】 明确叶际微生物对槟榔黄化病APV1病毒入侵的响应，为槟榔叶际微生态的研究、优异生防资源的挖掘及槟榔黄化病的绿色防控提供理论依据和技术支持。 【方法】 分别采集健康、轻度发病及重度发病槟榔叶片，通过高通量测序技术和生物信息学方法比较叶际微生物的群落结构与多样性并分析功能差异。 【结果】 槟榔叶际优势细菌门为放线菌门(Actinobacteriota)、变形菌门(Proteobacteria)、酸杆菌门(Acidobacteriota)、厚壁菌门(Firmicutes)和黏球菌门(Myxococcota)，优势真菌门为子囊菌门(Ascomycota)和担子菌门(Basidiomycota)。随着发病程度的增加，槟榔叶际细菌丰富度先升后降，真菌丰富度先降后升；细菌和真菌多样性均呈先升后降的趋势。厚壁菌门(Firmicutes)和担子菌门(Basidiomycota)作为轻度发病槟榔的标志物种，其相对丰度与α多样性变化趋势一致。健康与不同发病程度槟榔叶际微生物功能均发生了不同程度的变化，其中重度发病槟榔的环境信息处理功能显著高于健康槟榔；共生营养型(symbiotroph)的相对丰度极显著高于健康槟榔。 【结论】 槟榔黄化病显著改变了叶际微生物群落结构与多样性，且在发病初期变化较大，说明槟榔可能通过招募有益微生物、调控细胞代谢、生化反应、进行自身免疫等方式来抵御APV1病毒侵染。

槟榔  /  黄化病  /  叶际微生物  /  群落结构  /  多样性

[Objective] To clarify phyllosphere microbial responses to the invasion of areca palm velarivirus 1 (APV1), a virus causing yellow leaf disease of areca (Areca catechu), and provide a theoretical basis and technical support for the study of phyllosphere micro-ecology, exploration of excellent biocontrol resources, and green prevention and control of yellow leaf disease of areca. [Methods] We collected healthy leaves, mildly diseased leaves, and severely diseased leaves of areca. The phyllosphere microbial community structure and diversity were compared by high-throughput sequencing and bioinformatics methods. Furthermore, functional differences of phyllosphere microbial communities were analyzed. [Results] The dominant bacterial phyla in the phyllosphere of areca included Actinobacteriota, Proteobacteria, Acidobacteriota, Firmicutes, and Myxococcota, while the dominant fungal phyla were Ascomycota and Basidiomycota. As the disease became increasingly severe, bacterial richness initially increased then decreased while fungal richness initially decreased then increased. However, both bacterial diversity and fungal diversity showed a trend of first increasing and then decreasing. Firmicutes and Basidiomycota served as indicators of mildly diseased areca, with the relative abundance showing consistent trends with alpha diversity. The healthy plants and the diseased plants showed different phyllosphere microbial functions. Specifically, the environmental information processing function was significantly higher in severely diseased areca plants than in healthy ones. Additionally, the relative abundance of symbiotroph fungi in the phyllosphere were significantly higher in severely diseased areca plants than in healthy ones. [Conclusion] The yellow leaf disease significantly alters the phyllosphere microbial community structure and diversity of areca, with greater changes during the early disease stage. This suggests that areca may defend against APV1 infection by recruiting beneficial microorganisms, regulating cellular metabolism and biochemical reactions, and activating autoimmunity.

Areca catechu  /  yellow leaf disease  /  phyllosphere microorganism  /  community structure  /  diversity
马瑞, 王贞霖, 芮凯. 槟榔黄化病叶际微生物群落结构与多样性. 微生物学报, 2025 , 65 (8) : 3600 -3614 . DOI: 10.13343/j.cnki.wsxb.20250039
Rui MA, Zhenlin WANG, Kai RUI. Phyllosphere microbial community structure and diversity of Areca catechu with yellow leaf disease[J]. Acta Microbiologica Sinica, 2025 , 65 (8) : 3600 -3614 . DOI: 10.13343/j.cnki.wsxb.20250039
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槟榔(Areca catechu L.)属棕榈科多年生常绿乔木，主要分布在亚洲、非洲、欧洲和中美洲的热带及亚热带边缘地区[1]，是我国四大南药(槟榔、益智、砂仁、巴戟)之首[2]，具有抗疲劳、抗氧化、抗抑郁、抗炎镇痛和利尿等多种功能，并于1953年被列入《中华人民共和国药典》[3-5]。我国槟榔主要分布在海南、云南和台湾省，其中海南槟榔种植面积和总产量均占全国的95%以上[6]。目前，槟榔已成为海南230多万农民的主要经济来源，在海南实施乡村振兴战略、做强做优热带特色高效农业和建设国家生态文明试验区中发挥着举足轻重的作用[7]。槟榔黄化病是一种传染性疾病，病害症状开始于树冠中下层叶片，从叶尖逐渐变黄，发病叶片呈叶脉绿色、叶肉黄色的不均匀黄化，黄化与绿色部位交界明显，随后黄化症状扩展到上层叶片，新叶发育不良，冠幅明显减小，出现“束顶”症状，最终导致植株死亡，造成槟榔大面积减产甚至绝产[8]。研究证实APV1病毒感染与海南槟榔黄化病高度相关[9]，但目前尚缺少针对病毒特异性的有效化学药剂，导致槟榔黄化病传播较快且较广，严重影响了槟榔产业的可持续发展[10]。
叶际微生物在保护寄主植物免受病原菌侵染方面具有至关重要的作用[11-13]，Vogel等[14]对拟南芥叶际200多种细菌的植物保护能力进行了系统性分析，发现约10%的菌株通过多重相互作用保护拟南芥免受假单胞杆菌侵袭，约10%的菌株显示出中等程度的保护作用，其植物保护机制有多种。Ma等[15]从烟草叶际分离出了群体感应猝灭细菌，主要包括芽孢杆菌属、不动杆菌属和假单胞菌属等，其中79%的菌株都具有降解N-酰基高丝氨酸内酯(N-acylhomoserine lactone, AHL)信号分子的内酯酶活性，可作为潜在的生物防治剂抑制烟草病原菌。Berg和Koskella[16]发现，接种番茄叶际相关微生物群可以影响细菌斑点病丁香假单胞菌的定殖，但不同微生物群落的保护程度不同，且取决于所施用的微生物群接种剂量和植株的无机营养状况。目前，关于槟榔叶际微生物组的研究仍较为有限。为深入探究槟榔黄化病对叶际微生物群落的影响，发掘潜在的优良生防资源，并推进槟榔黄化病的绿色防控策略，本研究采用高通量测序技术系统分析了健康槟榔与不同发病程度槟榔叶际微生物的群落结构及多样性特征，并进一步探讨了其功能差异及潜在机制。
1 材料与方法
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1.1 材料
供试样品采自海南省定安县龙河镇鸭塘村槟榔园(19°23′N，110°13′E)，槟榔品种为海南本地种，树龄约10年，果形为椭圆形，节间8-15 cm，有效叶片6-7片。试验设置3组处理，分别为健康槟榔(JK)、轻度发病槟榔(MD)和重度发病槟榔(SD)。健康槟榔是指绿色叶片数大于或等于5片，只有最下面1片老叶黄化或有病斑的植株；轻度发病槟榔是指绿色叶片数大于或等于4片的植株；重度发病槟榔是指绿色叶片数少于或等于2片的植株。随机选择长势相近的槟榔植株，使用经乙醇消毒的高枝剪采集树冠中层叶片，观察挑选干净无虫卵的小裂叶放入无菌袋中密封保存，用干冰运输至实验室，冻存于-80 ℃冰箱中备用。每处理5个重复，每个重复的叶片均来源于同一株树。
1.2 基因组DNA提取
按照张怀文等[17]的方法检测病原，根据检测结果挑选阴性且无症状的叶片作为健康组(CK)样品，阳性且黄化症状明显的叶片作为感病组(MD/SD)样品进行后续研究。每个重复称取75 g槟榔叶片，在超净工作台中使用无菌剪刀剪成3 cm×4 cm的小块，置于含有750 mL无菌水的三角瓶中，并添加一定量的表面活性剂Silwet L-77[18]，用灭菌膜封口后在25 ℃、200 r/min的摇床中振荡20 min，将微生物细胞从叶片表面分离，然后在无菌环境中使用真空抽滤装置将振荡液中的微生物收集到0.22 μm孔径滤膜上[19]。使用SPINeasy DNA Kit for Plant (MP Biomedicals公司)提取槟榔叶际微生物基因组DNA，保存于-20 ℃[20]。
1.3 PCR扩增及高通量测序
分别用通用引物338F (5′-ACTCCTACGGG AGGCAGCA-3′)/806R (5′-GGACTACHVGGGT WTCTAAT-3′)和ITS1F (5′-CTTGGTCATTTAGA GGAAGTAA-3′)/ITS2 (5′-GCTGCGTTCTTCATC GATGC-3′)对细菌16S rRNA基因的V3-V4区与真菌ITS1区进行扩增[20]。PCR反应体系(10 μL)：KOD FX Neo Buffer 5 μL，dNTPs 2 μL，上、下游引物(10 μmol/L)各0.3 μL，KOD FX Neo (1.0 U/μL) 0.2 μL，DNA模板0.5 μL，ddH2O补至10 μL。PCR扩增程序：95 ℃预变性5 min；95 ℃变性30 s，50 ℃退火30 s，72 ℃延伸40 s，25/30个循环(细菌/真菌)；72 ℃终延伸7 min。扩增产物经纯化、定量和均一化形成测序文库，质检合格后用Illumina NovaSeq 6000进行测序。
1.4 数据分析
首先使用Trimmomatic v0.33软件对原始数据进行质量过滤，然后使用Cutadapt 1.9.1软件进行引物序列的识别与去除，再使用QIIME 2中的dada2方法进行去噪，以获得的最终序列数的0.005%作为阈值进行扩增子序列变体(amplicon sequence variant, ASV)的划分和聚类，分别以Silva.138和UNITE作为细菌和真菌参考数据库，使用朴素贝叶斯分类器对ASV进行分类学注释，根据注释结果筛除叶绿体和线粒体来源的序列，以保证分析结果的准确性。使用QIIME软件对样品α多样性指数进行评估，包括物种丰富度(Chao1指数)和物种多样性(Shannon指数)，基于Bray Curtis算法进行β多样性分析，采用非参数统计方法Kruskal-Wallis秩和检验进行组间差异显著性分析，使用Tax4Fun2 v1.1.5软件预测细菌功能，Funguild v1.0软件预测真菌功能，利用R语言工具绘制稀释曲线图、Venn图、物种组成柱状图、物种功能柱状图等。以上分析均在百迈克云平台(https://international.biocloud.net)上完成。
2 结果与分析
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2.1 测序数据质量评估
细菌原始测序数据质控后共产生79 732条高质量序列，经过去噪、双端序列拼接并去除嵌合体序列后，最终得到62 491条有效序列，平均为4 166条。真菌原始测序数据质控后共产生514 145条高质量序列，经过去噪、双端序列拼接并去除嵌合体序列后，最终得到496 870条有效序列，平均为33 125条。稀释曲线展示了不同样本间多样性的差异，各样本的稀释曲线趋于平缓，说明测序深度已经基本覆盖到样本中的所有物种，测序数据量足以反映样本中的物种多样性(图1)。
2.2 不同发病程度槟榔叶际微生物ASV分析
上述序列经聚类后分别得到1 175个细菌ASVs和3 614个真菌ASVs。不同组间细菌ASVs数排序为：MD (474个)>JK (435个)>SD (373个)；真菌ASVs数排序为：JK (1 512个)>SD (1 478个)>MD (1 349个)。其中，轻度发病槟榔(MD)含有的细菌ASVs总数和独有ASVs数均为最多，但真菌ASVs总数和独有ASVs数均为最少。健康与不同发病程度槟榔样品间共有的细菌ASVs和真菌ASVs分别为24个和172个，占各自ASVs总数的2.04%和4.76% (图2)。
2.3 不同发病程度槟榔叶际物种分类
分类学注释结果显示，槟榔叶际细菌归属于24门45纲98目174科324属；真菌归属于10门34纲91目213科437属。在门水平上(图3)，槟榔叶际细菌主要包括放线菌门(Actinobacteriota)、变形菌门(Proteobacteria)、酸杆菌门(Acidobacteriota)、厚壁菌门(Firmicutes)和黏球菌门(Myxococcota)(相对丰度大于1.00%)。随着病情等级的增加，放线菌门(Actinobacteriota)(27.15%-40.19%)、变形菌门(Proteobacteria)(22.94%-28.94%)、酸杆菌门(Acidobacteriota)(13.67%-20.04%)和黏球菌门(Myxococcota)(1.15%-10.99%)的相对丰度呈先降后升的趋势，厚壁菌门(Firmicutes)(2.50%-30.69%)呈先升后降的趋势，虽然菌群的相对丰度发生了不同程度的变化，但不同组间均无显著差异。槟榔叶际真菌主要包括子囊菌门(Ascomycota)和担子菌门(Basidiomycota)(相对丰度大于1.00%)。随着病情等级的增加，子囊菌门(Ascomycota)(73.08%-87.58%)呈先降后升的趋势，担子菌门(Basidiomycota)(11.44%-26.29%)呈先升后降的趋势。
在属水平上(图4)，槟榔叶际细菌中Bryocella和放线孢菌属(Actinomycetospora)为共有优势属(相对丰度大于5.00%)。健康槟榔样品(JK)中unclassified_Diplorickettsiaceae、P3OB_42、Edaphobacter、杀雄菌属(Arsenophonus)、芽孢杆菌属(Bacillus)和间孢囊菌科未知分类属(unclassified_Intrasporangiaceae)的相对丰度更高；发病槟榔样品(MD、SD)中放线孢菌属(Actinomycetospora)、柄细菌科未知分类属(unclassified_Caulobacteraceae)、泛菌属(Pantoea)和假诺卡氏菌属(Pseudonocardia)的相对丰度更高。槟榔叶际真菌中球腔菌科未知分类属(unclassified_Mycosphaerellaceae)和担子菌门未知分类属(unclassified_Basidiomycota)为共有优势属(相对丰度大于5.00%)。健康槟榔样品(JK)中，球腔菌科未知分类属(unclassified_Mycosphaerellaceae)和Zasmidium的相对丰度更高；发病槟榔样品(MD、SD)中，担孢酵母属(Erythrobasidium)、座囊菌纲未知分类属(unclassified_Dothideomycetes)、担子菌门未知分类属(unclassified_Basidiomycota)、子囊菌门未知分类属(unclassified_Ascomycota)、畸球腔菌科未知分类属(unclassified_Teratosphaeriaceae)、刺盾炱目未知分类属(unclassified_Chaetothyriales)和Letendraea的相对丰度更高。
2.4 不同发病程度槟榔叶际微生物α多样性分析
Chao1指数和Shannon指数分别用于衡量物种丰富度和物种多样性。随发病程度的增加，槟榔叶际细菌群落Chao1指数呈先升后降的趋势，但不同组间无显著差异；Shannon指数也呈先升后降的趋势，轻度发病槟榔叶际细菌群落多样性最高，与健康槟榔差异显著，与重度发病槟榔差异极显著。槟榔叶际真菌群落Chao1指数随发病程度的增加呈先降后升的趋势，而Shannon指数呈先升后降的趋势，健康槟榔与轻度发病槟榔之间的丰富度和多样性均具有显著差异。除此之外，健康槟榔与重度发病槟榔叶际微生物的丰富度和多样性均无显著差异(图5)。
2.5 不同发病程度槟榔叶际微生物β多样性分析
对健康和不同发病程度的槟榔样本进行基于Bray-Curtis距离的主坐标分析(PCoA)，结果显示细菌第一主坐标轴和第二主坐标轴的解释度分别为16.52%和15.19%，真菌第一主坐标轴和第二主坐标轴的解释度分别为21.18%和16.15% (图6)。同组样本均能较紧密地结合在一起，有很高的相似性，不同组样本可以明显地区分开。进一步用非参数检验法(analysis of similarities, ANOISM)分析得P<0.01。UPGMA聚类分析结果与PCoA结果一致(图7)。说明槟榔叶际微生物群落在3个不同组间均具有极显著差异。
2.6 不同发病程度槟榔叶际物种组成差异分析
线性判别分析(linear discriminant analysis effect size, LEfSe)揭示了健康和不同发病程度槟榔叶际的特有生物标记物，即特有的丰富物种(图8、图9)。在属水平上，健康槟榔(JK)叶际的细菌生物标记物为unclassified_Diplorickettsiaceae和Edaphobacter，真菌的生物标记物为球腔菌科未知分类属(unclassified_Mycosphaerellaceae)和Leptoxyphium；轻度发病槟榔(MD)叶际细菌的生物标记物为埃氏菌属-志贺氏菌属(Escherichia_Shigella)、Agathobacter、巨单胞菌属(Megamonas)和小杆菌属(Dialister)，真菌的生物标记物为Bimuria、Kockovaella和虫草科未知分类属(unclassified_Cordycipitaceae)；重度发病槟榔(SD)叶际细菌的生物标记物为Amnibacterium和孢囊杆菌属(Cystobacter)，真菌的生物标记物为假尾孢属(Pseudocercospora)、Hermetothecium、多孔菌目未知分类属(unclassified_Polyporales)、Pyrenochaetopsis、Letendraea和Neoacrodontiella。
2.7 不同发病程度槟榔叶际微生物功能预测
基于KEGG数据库对槟榔叶际微生物的基因进行功能注释，在一级功能层级上，槟榔叶际细菌主要分布于6类功能通路，分别为代谢(metabolism) (76.01%-78.43%)、环境信息处理(environmental information processing) (9.23%-10.47%)、细胞过程(cellular processes) (4.79%-5.73%)、遗传信息处理(genetic information processing) (3.72%-4.33%)、人类疾病(human diseases) (2.13%-2.54%)和有机系统(organismal systems) (1.44%-1.62%)，其中重度发病槟榔(SD)的环境信息处理功能显著高于健康槟榔(JK) (图10)。进一步对二级功能进行分析，结果表明健康槟榔(JK)与重度发病槟榔(SD)在全局和概述图谱(global and overview maps)、氨基酸代谢(amino acid metabolism)上存在显著差异，在信号传导(signal transduction)上存在极显著差异；轻度发病槟榔(MD)与重度发病槟榔(SD)在信号传导(signal transduction)上存在显著差异，在碳水化合物代谢(carbohydrate metabolism)上存在极显著差异(图11)。除上述提到的功能外，其他功能均无显著差异。
FunGuild真菌功能预测结果(图12)表明，槟榔叶际真菌主要分布于3类功能类群，分别为病理营养型(pathotroph) (44.53%-51.02%)、腐生营养型(saprotroph) (45.56%-52.07%)和共生营养型(symbiotroph) (1.18%-3.42%)。其中重度发病槟榔(SD)叶际共生营养型(symbiotroph)的相对丰度极显著高于健康槟榔(JK)，病理营养型(pathotroph)的相对丰度显著高于轻度发病槟榔(MD)，而腐生营养型(saprotroph)的相对丰度显著低于轻度发病槟榔(MD)。进一步细分为若干guilds后，随发病程度的增加，内生菌(endophyte)、地衣寄生菌(lichen parasite)、木质腐生菌(wood saprotroph)和排泄物腐生菌(dung saprotroph)的相对丰度逐渐上升。重度发病槟榔(SD)中内生菌(endophyte)和地衣寄生菌(lichen parasite)的相对丰度极显著高于健康槟榔(JK)。
3 讨论
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植物叶际中含有大量的微生物，这些微生物为植物提供了必要的营养物质，影响植物的生长发育和代谢活动。叶际微生物可以通过激素刺激或改善营养物质获取直接促进植物生长，也可以通过竞争、拮抗以及诱导植物系统抗性平衡叶际菌群，间接保护宿主抵御病原体的侵染[21-22]。本研究基于高通量测序技术，从微观层面解析了健康槟榔与感染黄化病槟榔叶际微生物的异同，并揭示了不同发病程度槟榔叶际微生物的群落结构与多样性。由于槟榔黄化病的进程非常缓慢，从感病初期到重病期通常需要几年的时间，研究同一株槟榔不同发病期的叶际微生物差异需耗费大量时间，且田间采样环境等因素难以控制，因此本研究以发病程度的轻重代表发病时期的不同阶段。
相对丰度分析表明，槟榔叶际优势细菌门为放线菌门(Actinobacteriota)、变形菌门(Proteobacteria)、酸杆菌门(Acidobacteriota)、厚壁菌门(Firmicutes)和黏球菌门(Myxococcota)，优势真菌门为子囊菌门(Ascomycota)和担子菌门(Basidiomycota)，这与前人对烟草、葡萄、南瓜等叶际微生物的研究结论相似[23-25]。在槟榔黄化病发生初期，槟榔叶际细菌丰富度逐渐增加，真菌丰富度逐渐下降，细菌和真菌多样性均逐渐增加，且轻度发病槟榔的Shannon指数显著高于健康槟榔；当病害发展到后期，叶际微生物丰富度和多样性又逐渐下降。整个发病过程中，叶际细菌和真菌多样性均呈先升后降的趋势，但丰富度的变化却不一致。基于Bray-Curtis距离的主坐标分析(PCoA)和UPGMA聚类分析表明健康与不同发病程度槟榔叶际微生物存在极显著差异。在门水平上，厚壁菌门(Firmicutes)和担子菌门(Basidiomycota)与α多样性变化趋势一致，随着病情发展在轻度发病槟榔中相对丰度上升至最高，在重度发病槟榔中相对丰度又有所下降。LEfSe分析也表明轻度发病槟榔的标志物包括厚壁菌门(Firmicutes)和担子菌门(Basidiomycota)。不同属的相对丰度随病情的发展均发生了不同程度的变化，但由于数据库注释信息有限，仍然有较多的物种未被识别到。上述结果与Zhang等[26]综合微生物组学和代谢组学研究槟榔叶片褪绿的生理机制有所不同，因其未进行病原检测，不能证实是由APV1病毒侵染造成的槟榔黄化病，可能是由于生理性原因导致槟榔植株自身分泌的次生代谢物质发生改变，进而影响了定殖在叶际的微生物群落组成和结构。
研究表明，植物微生物组的变化不仅是植物的被动反应，而是作为共同进化的结果，当植物经历生物或非生物胁迫时，可能会采用“呼救”策略从环境中招募有益的微生物，主动寻求与微生物的合作以缓解胁迫，这种植物与微生物的相互作用被认为是维持植物健康的关键[27-28]。由此推测在槟榔黄化病发生初期叶际微生物会迅速对APV1病毒的入侵作出响应，通过招募大量厚壁菌门(Firmicutes)或担子菌门(Basidiomycota)的有益微生物定殖来抵抗病原菌。在这个过程中叶际微生物的多样性增加，微生态平衡被破坏，丰富度会出现波动。随着发病程度越来越严重，叶片上有限的营养物质和生存空间不断降低，微生物间的竞争加剧，最终导致微生物丰富度降低。
叶际微生物在定殖积累过程中常发挥自身特定的生理功能，与其群落组成及结构息息相关[29-30]。本研究中细菌功能预测发现感病槟榔的信号传导功能(signal transduction)大于健康槟榔，且在发病初期达到最大，说明槟榔在发病初期就开始通过多种信号传导通路将细胞外的分子信号传递到细胞内，并引发一系列的生化反应，从而实现细胞对外界病原菌入侵的响应和调节。真菌功能预测发现病理营养型(pathotroph)真菌在轻度发病槟榔中有所下降，在重度发病槟榔中又显著升高；腐生营养型(saprotroph)真菌呈先升后降的趋势，共生营养型(symbiotroph)真菌持续上升，说明病害刚开始发生时死亡的宿主细胞大量增加，通过降解死亡细胞获取营养的腐生营养型(saprotroph)真菌也随之上升。同时，槟榔通过“呼救”策略招募有益微生物来对抗病原菌，使病理营养型(pathotroph)真菌短暂下降。随着病情进一步发展，后期可能会合并其他病害，导致病理营养型(pathotroph)真菌再次升高。通过与宿主细胞交换资源来获取营养的共生营养型(symbiotroph)真菌也不断上升。
综上所述，槟榔叶际微生物在黄化病发病初期就作出了多种反应来抵抗病原菌的入侵，包括招募有益微生物、调控细胞代谢、引发生化反应、进行自身免疫等，这也说明了防控槟榔黄化病的最佳时期是未发病时至发病前期，通过调节叶际微生物群落的特定组成以拮抗病原体感染可能成为防控槟榔黄化病的新策略。
4 结论
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本研究发现由APV1病毒引起的槟榔黄化病会影响叶际微生物的组成结构和功能，且健康和不同发病程度槟榔叶际微生物存在极显著差异。槟榔叶际微生物中优势细菌门为放线菌门(Actinobacteriota)、变形菌门(Proteobacteria)、酸杆菌门(Acidobacteriota)、厚壁菌门(Firmicutes)和黏球菌门(Myxococcota)，优势真菌门为子囊菌门(Ascomycota)和担子菌门(Basidiomycota)。随着发病程度的增加，厚壁菌门(Firmicutes)和担子菌门(Basidiomycota)的相对丰度均呈先升后降的趋势，与α多样性变化趋势一致。健康和不同发病程度槟榔叶际均有特定的生物标记物，细菌和真菌功能也发生了不同程度的变化。进一步说明了槟榔叶际可以通过招募有益微生物来抵抗病原菌的侵染，为槟榔黄化病的防控提供了新思路。
基金
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文献
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2025年第65卷第8期
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doi: 10.13343/j.cnki.wsxb.20250039
  • 接收时间：2025-01-15
  • 首发时间：2026-02-06
  • 出版时间：2025-08-04
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  • 收稿日期：2025-01-15
  • 录用日期：2025-03-21
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Earmarked Fund for HNARS
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    1.海南省农业科学院植物保护研究所，海南省农业科学院农产品质量安全与标准研究中心，海南省植物病虫害防控重点实验室，农业农村部海口作物有害生物科学观测实验站，海南 海口
    2.海南省农业科学院三亚研究院，海南 三亚

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2种不同金属材料的力学参数
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Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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