Assessing microbial diversity in anthers of <i>Eriobotrya japonica</i> (Thunb.) Lindl. based on high-throughput sequencing

Gao Feng; Deng Guocui; Zhang Wu; Zhang Yechi; Gong Yanbing

doi:10.11913/PSJ.2095-0837.24270

Plant Science Journal > 2025 > 43(1): 32-40. > DOI: 10.11913/PSJ.2095-0837.24270 CSTR: 32231.14.PSJ.2095-0837.24270

Gao F，Deng GC，Zhang W，Zhang YC，Gong YB. Assessing microbial diversity in anthers of Eriobotrya japonica (Thunb.) Lindl. based on high-throughput sequencing[J]. Plant Science Journal，2025，43（1）：32−40. DOI: 10.11913/PSJ.2095-0837.24270

Citation:

PDF (588 KB)

Assessing microbial diversity in anthers of Eriobotrya japonica (Thunb.) Lindl. based on high-throughput sequencing

1.
State Key Laboratory of Hybrid Rice, Key Laboratory of Biodiversity and Environment on the Qinghai-Tibet Plateau, Ministry of Education, College of Sciences, Wuhan University, Wuhan 430072, China
2.
Xinjiang Key Laboratory of Biological Resources and Genetic Engineering, College of Life Science and Technology, Xinjiang University, Urumqi 830046, China

More Information

Received Date: November 09, 2024
Accepted Date: November 29, 2024

Graphical Abstract

Abstract

Abstract

Fruit trees, vital to global agriculture, depend heavily on pollinators to facilitate successful reproduction and ensure optimal yield. Microorganisms associated with anthers can influence pollen viability, and their community composition may be affected by pollinator activity. While understanding the diversity and community assembly patterns of these microorganisms has potential implications for enhancing the reproductive fitness of fruit trees, research in this area remains relatively scarce. This study employed high-throughput sequencing to analyze the diversity and community structure of fungi and bacteria on the anthers of loquat (Eriobotrya japonica (Thunb.) Lindl.) before (bagged group) and after (nature group) pollinator visitation. Results showed that pollinator visitation had no significant effect on the diversity or composition of anther microbiomes. In the bagged group, dominant fungal taxa included Cladosporiaceae and Mycosphaerellaceae, whereas Cladosporiaceae and Metschnikowiaceae were dominant in the nature group. Bacterial communities in both groups were also dominated by Alcaligenaceae and Erwiniaceae. These findings indicate that the microbial community composition within loquat anthers is inherently stable and largely unaffected by pollinator activity.
- Pollinator visits,
- Anther microbes,
- High-throughput sequencing technology,
- Microbial composition

FullText(HTML)

References (57)

References

[1]	Theodorou P,Radzevičiūtė R,Lentendu G,Kahnt B,Husemann M,et al. Urban areas as hotspots for bees and pollination but not a panacea for all insects[J]. Nat Commun,2020,11(1):576. doi: 10.1038/s41467-020-14496-6
[2]	Didham RK,Basset Y,Collins CM,Leather SR,Littlewood NA,et al. Interpreting insect declines:seven challenges and a way forward[J]. Insect Conserv Diver,2020,13(2):103−114. doi: 10.1111/icad.12408
[3]	Hallmann CA,Sorg M,Jongejans E,Siepel H,Hofland N,et al. More than 75 percent decline over 27 years in total flying insect biomass in protected areas[J]. PLoS One,2017,12(10):e0185809. doi: 10.1371/journal.pone.0185809
[4]	Sánchez-Bayo F,Wyckhuys KAG. Worldwide decline of the entomofauna:a review of its drivers[J]. Biol Conserv,2019,232:8−27. doi: 10.1016/j.biocon.2019.01.020
[5]	Lister BC,Garcia A. Climate-driven declines in arthropod abundance restructure a rainforest food web[J]. Proc Natl Acad Sci USA,2018,115(44):E10397−E10406.
[6]	Tong ZY,Wu LY,Feng HH,Zhang M,Armbruster WS,et al. New calculations indicate that 90% of flowering plant species are animal-pollinated[J]. Natl Sci Rev,2023,10(10):nwad219. doi: 10.1093/nsr/nwad219
[7]	Steffan SA,Dharampal PS,Kueneman JG,Keller A,Argueta-Guzmán MP,et al. Microbes,the 'silent third partners' of bee-angiosperm mutualisms[J]. Trends Ecol Evol,2024,39(1):65−77. doi: 10.1016/j.tree.2023.09.001
[8]	Kwon Y,Lee JT,Kim HS,Jeon C,Kwak YS. Comparative tomato flower and pollinator hive microbial communities[J]. J Plant Dis Prot,2018,125(1):115−119. doi: 10.1007/s41348-017-0090-z
[9]	Eisdcowitch D,Kevan PG,Lachance MA. The nectar-inhabiting yeasts and their effect on pollen germination in common milkweed,Asclepias syriaca L.[J]. Isr J Bot,1990,39(1-2):217−225.
[10]	Eisikowitch D,Lachance MA,Kevan PG,Willis S,Collins-Thompson DL. The effect of the natural assemblage of microorganisms and selected strains of the yeast Metschnikowia reukaufii in controlling the germination of pollen of the common milkweed Asclepias syriaca[J]. Can J Bot,1990,68(5):1163−1165. doi: 10.1139/b90-147
[11]	Christensen SM,Munkres I,Vannette RL. Nectar bacteria stimulate pollen germination and bursting to enhance microbial fitness[J]. Curr Biol,2021,31(19):4373−4380.
[12]	Canto A,Herrera CM,Medrano M,Pérez R,García IM. Pollinator foraging modifies nectar sugar composition in Helleborus foetidus (Ranunculaceae):an experimental test[J]. Am J Bot,2008,95(3):315−320. doi: 10.3732/ajb.95.3.315
[13]	Peay KG,Belisle M,Fukami T. Phylogenetic relatedness predicts priority effects in nectar yeast communities[J]. Proc Roy Soc B Biol Sci,2012,279(1729):749−758.
[14]	Rering CC,Beck JJ,Hall GW,McCartney MM,Vannette RL. Nectar-inhabiting microorganisms influence nectar volatile composition and attractiveness to a generalist pollinator[J]. New Phytol,2018,220(3):750−759. doi: 10.1111/nph.14809
[15]	Yang M,Deng GC,Gong YB,Huang SQ. Nectar yeasts enhance the interaction between Clematis akebioides and its bumblebee pollinator[J]. Plant Biol,2019,21(4):732−737. doi: 10.1111/plb.12957
[16]	Herrera CM,de Vega C,Canto A,Pozo MI. Yeasts in floral nectar:a quantitative survey[J]. Ann Bot,2009,103(9):1415−1423. doi: 10.1093/aob/mcp026
[17]	Shade A,McManus PS,Handelsman J. Unexpected diversity during community succession in the apple flower microbiome[J]. Mbio,2013,4(2):e00602−12.
[18]	Aleklett K,Hart M,Shade A. The microbial ecology of flowers:an emerging frontier in phyllosphere research[J]. Botany,2014,92(4):253−266. doi: 10.1139/cjb-2013-0166
[19]	Canto A,Herrera CM,Rodriguez R. Nectar-living yeasts of a tropical host plant community:diversity and effects on community-wide floral nectar traits[J]. PeerJ,2017,5:e3517. doi: 10.7717/peerj.3517
[20]	Von Arx M,Moore A,Davidowitz G,Arnold AE. Diversity and distribution of microbial communities in floral nectar of two night-blooming plants of the Sonoran desert[J]. PLoS One,2019,14(12):e0225309. doi: 10.1371/journal.pone.0225309
[21]	De Vega C,Álvarez-Pérez S,Albaladejo RG,Steenhuisen SL,Lachance MA,et al. The role of plant-pollinator interactions in structuring nectar microbial communities[J]. J Ecol,2021,109(9):3379−3395. doi: 10.1111/1365-2745.13726
[22]	Vorholt JA. Microbial life in the phyllosphere[J]. Nat Rev Microbiol,2012,10(12):828−840. doi: 10.1038/nrmicro2910
[23]	Rebolleda Gómez M,Ashman TL. Floral organs act as environmental filters and interact with pollinators to structure the yellow monkeyflower (Mimulus guttatus) floral microbiome[J]. Mol Ecol,2019,28(23):5155−5171. doi: 10.1111/mec.15280
[24]	Russell AL,Rebolleda-Gómez M,Shaible TM,Ashman TL. Movers and shakers:bumble bee foraging behavior shapes the dispersal of microbes among and within flowers[J]. Ecosphere,2019,10(5):e02714. doi: 10.1002/ecs2.2714
[25]	周肖霄,张彦文,赵骥民,李竹月. 花部微生物生态学研究进展[J]. 植物科学学报,2023,41(1):121−127. doi: 10.11913/PSJ.2095-0837.22036 Zhou XX,Zhang YW,Zhao JM,Li ZY. Advances in floral microbial ecology[J]. Plant Science Journal,2023,41(1):121−127. doi: 10.11913/PSJ.2095-0837.22036
[26]	Cariñanos P,Casares-Porcel M. Urban green zones and related pollen allergy:a review. Some guidelines for designing spaces with low allergy impact[J]. Landscape Urban Plann,2011,101(3):205−214. doi: 10.1016/j.landurbplan.2011.03.006
[27]	Oldenburg M,Petersen A,Baur X. Maize pollen is an important allergen in occupationally exposed workers[J]. J Occup Med Toxicol,2011,6:32. doi: 10.1186/1745-6673-6-32
[28]	Abbate JL,Gladieux P,Hood ME,de Vienne DM,Antonovics J,et al. Co-occurrence among three divergent plant-castrating fungi in the same silene host species[J]. Mol Ecol,2018,27(16):3357−3370. doi: 10.1111/mec.14805
[29]	Hartmann FE,Rodríguez de la Vega RC,Carpentier F,Gladieux P,Cornille A,et al. Understanding adaptation,coevolution,host specialization,and mating system in castrating anther-smut fungi by combining population and comparative genomics[J]. Annu Rev Phytopathol,2019,57:431−457. doi: 10.1146/annurev-phyto-082718-095947
[30]	Alexander HM. Epidemiology of anther-smut infection of Silene alba caused by Ustilago violacea:patterns of spore deposition and disease incidence[J]. J Ecol,1990,78(1):166−179. doi: 10.2307/2261043
[31]	Jennersten O. Insect dispersal of fungal disease:effects of Ustilago infection on pollinator attraction in Viscaria vulgaris[J]. Oikos,1988,51(2):163−170. doi: 10.2307/3565638
[32]	Curran HR,Roets F,Dreyer LL. Anther-smut fungal infection of South African Oxalis species:spatial distribution patterns and impacts on host fecundity[J]. South Afr J Bot,2009,75(4):807−815. doi: 10.1016/j.sajb.2009.08.004
[33]	Ambika Manirajan B,Ratering S,Rusch V,Schwiertz A,Geissler-Plaum R,et al. Bacterial microbiota associated with flower pollen is influenced by pollination type,and shows a high degree of diversity and species-specificity[J]. Environ Microbiol,2016,18(12):5161−5174. doi: 10.1111/1462-2920.13524
[34]	Fang Q,Chen YZ,Huang SQ. Generalist passerine pollination of a winter-flowering fruit tree in central China[J]. Ann Bot,2012,109(2):379−384. doi: 10.1093/aob/mcr293
[35]	蔡平,包立军,相入丽,张璐. 中国枇杷主要病害发生规律及综合防治[J]. 中国南方果树,2005,34(3):47−50.
[36]	王继廉,李玉花. 枇杷病虫害防治要点[J]. 云南农业,2016(1):37−38.
[37]	Pozo MI,Herrera CM,Bazaga P. Species richness of yeast communities in floral nectar of southern Spanish plants[J]. Microbiol Ecol,2011,61(1):82−91. doi: 10.1007/s00248-010-9682-x
[38]	Pozo MI,Lachance MA,Herrera CM. Nectar yeasts of two southern Spanish plants:the roles of immigration and physiological traits in community assembly[J]. FEMS Microbiol Ecol,2012,80(2):281−293. doi: 10.1111/j.1574-6941.2011.01286.x
[39]	Smessaert J,van Geel M,Verreth C,Crauwels S,Honnay O,et al. Temporal and spatial variation in bacterial communities of "Jonagold" apple (Malus×domestica Borkh.) and "Conference" pear (Pyrus communis L.) floral nectar[J]. MicrobiologyOpen,2019,8(12):e918. doi: 10.1002/mbo3.918
[40]	Rering CC,Rudolph AB,Li QB,Read QD,Muñoz PR,et al. A quantitative survey of the blueberry (Vaccinium spp.) culturable nectar microbiome:variation between cultivars,locations,and farm management approaches[J]. FEMS Microbiol Ecol,2024,100(3):fiae020. doi: 10.1093/femsec/fiae020
[41]	Pozo MI,Herrera CM,Alonso C. Spatial and temporal distribution patterns of nectar-inhabiting yeasts:how different floral microenvironments arise in winter-blooming Helleborus foetidus[J]. Fungal Ecol,2014,11:173−180. doi: 10.1016/j.funeco.2014.06.007
[42]	Toju H,Vannette RL,Gauthier MPL,Dhami MK,Fukami T. Priority effects can persist across floral generations in nectar microbial metacommunities[J]. Oikos,2018,127(3):345−352. doi: 10.1111/oik.04243
[43]	Zemenick AT,Rosenheim JA,Vannette RL. Legitimate visitors and nectar robbers of Aquilegia formosa have different effects on nectar bacterial communities[J]. Ecosphere,2018,9(10):e02459. doi: 10.1002/ecs2.2459
[44]	Vokou D,Vareli K,Zarali E,Karamanoli K,Constantinidou HIA,et al. Exploring biodiversity in the bacterial community of the mediterranean phyllosphere and its relationship with airborne bacteria[J]. Microb Ecol,2012,64(3):714−724. doi: 10.1007/s00248-012-0053-7
[45]	Herrera CM,Canto A,Pozo MI,Bazaga P. Inhospitable sweetness:nectar filtering of pollinator-borne inocula leads to impoverished,phylogenetically clustered yeast communities[J]. Proc Roy Soc B Biol Sci,2010,277(1682):747−754.
[46]	Junker RR,Keller A. Microhabitat heterogeneity across leaves and flower organs promotes bacterial diversity[J]. FEMS Microbiol Ecol,2015,91(9):fiv097. doi: 10.1093/femsec/fiv097
[47]	Kosenko VN. Contributions to the pollen morphology and taxonomy of the Liliaceae[J]. Grana,1999,38(1):20−30. doi: 10.1080/001731300750044672
[48]	Debray R,Herbert RA,Jaffe AL,Crits-Christoph A,Power ME,Koskella B. Priority effects in microbiome assembly[J]. Nat Rev Microbiol,2022,20(2):109−121. doi: 10.1038/s41579-021-00604-w
[49]	Dhami MK,Hartwig T,Fukami T. Genetic basis of priority effects:insights from nectar yeast[J]. Proc Roy Soc B Biol Sci,2016,283(1840):20161455.
[50]	Wilson M,Lindow SE. Coexistence among epiphytic bacterial populations mediated through nutritional resource partitioning[J]. Appl Environ Microbiol,1994,60(12):4468−4477. doi: 10.1128/aem.60.12.4468-4477.1994
[51]	Belisle M,Peay KG,Fukami T. Flowers as islands:spatial distribution of nectar-inhabiting microfungi among plants of Mimulus aurantiacus,a Hummingbird-pollinated shrub[J]. Microb Ecol,2012,63(4):711−718. doi: 10.1007/s00248-011-9975-8
[52]	Hendry TA,Ligon RA,Besler KR,Fay RL,Smee MR. Visual detection and avoidance of pathogenic bacteria by Aphids[J]. Curr Biol,2018,28(19):3158−3164. e4.
[53]	Rering CC,Vannette RL,Schaeffer RN,Beck JJ. Microbial co-occurrence in floral nectar affects metabolites and attractiveness to a generalist pollinator[J]. J Chem Ecol,2020,46(8):659−667. doi: 10.1007/s10886-020-01169-3
[54]	Russell AL,Ashman TL. Associative learning of flowers by generalist bumble bees can be mediated by microbes on the petals[J]. Behav Ecol,2019,30(3):746−755. doi: 10.1093/beheco/arz011
[55]	Schaeffer RN,Rering CC,Maalouf I,Beck JJ,Vannette RL. Microbial metabolites elicit distinct olfactory and gustatory preferences in bumblebees[J]. Biol Lett,2019,15(7):20190132. doi: 10.1098/rsbl.2019.0132
[56]	Morris MM,Frixione NJ,Burkert AC,Dinsdale EA,Vannette RL. Microbial abundance,composition,and function in nectar are shaped by flower visitor identity[J]. FEMS Microbiol Ecol,2020,96(3):fiaa003. doi: 10.1093/femsec/fiaa003
[57]	Allard SM,Ottesen AR,Brown EW,Micallef SA. Insect exclusion limits variation in bacterial microbiomes of tomato flowers and fruit[J]. J Appl Microbiol,2018,125(6):1749−1760. doi: 10.1111/jam.14087

[1]	Zhou Xiao-Xiao, Zhang Yan-Wen, Zhao Ji-Min, Li Zhu-Yue. Advances in floral microbial ecology[J]. Plant Science Journal, 2023, 41(1): 121-127. DOI: 10.11913/PSJ.2095-0837.22036
[2]	Tong Ling, Lei Feng-Wei, Wu Yuan-Mi, Shen Xue-Li, Dong Shu-Bin, Mu Xian-Yun. Study on rhizosphere microorganism diversity of a myco-heterotrophic orchid endemic to North China, Holopogon pekinensis X. Y. Mu & Bing Liu[J]. Plant Science Journal, 2022, 40(3): 324-333. DOI: 10.11913/PSJ.2095-0837.2022.30324
[3]	QIU Hao, CHEN Jia-yang, LAI You-zhen, ZHANG Guo-yan, CUI Lang-jun, WEI Xi-ying. Relationships between endophytic structure, rhizosphere soil properties and aconite alkaloids accumulations in Aconitum carmichaelii Debx.[J]. Plant Science Journal, 2021, 39(6): 643-653. DOI: 10.11913/PSJ.2095-0837.2021.60643
[4]	Li Yong-Heng, Li Qian-Xi, Wu Jun-Jun, Cheng Xiao-Li. Soil microbial attributes at different spatial scales in deciduous broad-leaved forest in Qinling Mountains[J]. Plant Science Journal, 2020, 38(3): 335-346. DOI: 10.11913/PSJ.2095-0837.2020.30335
[5]	MU Jin-Hu, CHEN Yu-Ze, FENG Hui, LI Wen-Jian, ZHOU Li-Bin. A New Revolution in Crop Breeding: The Era of High-Throughput Phenomics[J]. Plant Science Journal, 2016, 34(6): 962-971. DOI: 10.11913/PSJ.2095-0837.2016.60962
[6]	GAO Shuang, LIU Xiao-Chen, DONG Zheng, LIU Mao-Yan, DAI Liang-Ying. Advance of Phyllosphere Microorganisms and Their Interaction with the Outside Environment[J]. Plant Science Journal, 2016, 34(4): 654-661. DOI: 10.11913/PSJ.2095-0837.2016.40654
[7]	ZHANG Tian-Han, WANG Jian-Ming, XIA Yan-Guo, ZHENG Chang-Long, LI Jing-Wen, JIA Xiao-Hong, WU Bo. Composition of Seed Plant Species and Flora Features in Different Areas of the Kumtag Desert of China[J]. Plant Science Journal, 2016, 34(1): 78-88. DOI: 10.11913/PSJ.2095-0837.2016.10078
[8]	MI Qi, LONG Zhi-Cheng, MUCHUKU John Kamau, CHEN Jin-Ming, WANG Qing-Feng. Development of SSR Markers in Giant Lobelia (Lobelia deckenii) Based on Next-generation High-throughput Sequencing[J]. Plant Science Journal, 2015, 33(6): 847-854. DOI: 10.11913/PSJ.2095-0837.2015.60847
[9]	LI Jian-Hua, WANG Wei, YAO Guo-Xing, WANG Dian-Pei. Composition of Bark Fiber of Wild Pteroceltis tatarinowii in Daguisi National Forest Park[J]. Plant Science Journal, 2012, 30(5): 511-518. DOI: 10.3724/SP.J.1142.2012.50511
[10]	NONG Shou-Qian, YANG Xiao-Bo, LI Dong-Hai, YANG Li-Rong, XU Zhong-Liang, CHEN Yu-Kai, LUO Zhao-Mei. Vegetation Composition in the Mangrove Forest Nature Protection Area of Qinglan,China[J]. Plant Science Journal, 2011, 1(4): 459-466.

Cited By

Cited by

Periodical cited type(12)

1.	张琦，蒲婷婷，王艺儒，胡银凤，李华威，韩卫娟，索玉静，傅建敏. 不同柿种质果实品质多样性评价. 中国农业大学学报. 2025(02): 61-71 .
2.	罗赛男，张文. 我国猕猴桃质量安全标准体系现状及建议. 食品安全质量检测学报. 2025(01): 243-249 .
3.	王宝趁. 不同猕猴桃品种果实品质比较研究. 现代农业科技. 2024(02): 140-143+164 .
4.	张慧艺，汪丽霞，吴伊静，毕旭灿，王刚，赵四清，徐昌杰，陈昆松. 18份胡柚种质果实品质分析与综合评价. 果树学报. 2024(06): 1033-1043 .
5.	李艺潇，陈建华，闫芳芳，焦子源，李纪军，马培芳. 韭菜种质资源营养与感官品质评价. 中国瓜菜. 2024(08): 109-116 .
6.	孔令硕，樊丁宇，靳娟，杨磊，郝庆，田嘉. 灰枣及其芽变品种果实品质评价. 现代农业科技. 2024(16): 119-123+131 .
7.	傅一凡，王周倩，邱栋梁，黄文俊，钟彩虹. 防雹网对‘东红’猕猴桃果实耐贮性和品质的影响. 植物科学学报. 2024(04): 533-542 . 本站查看
8.	黄文俊，王周倩，杨洁，张琦，钟彩虹. 不同干物质含量对金艳猕猴桃果实品质和感官评价的影响. 落叶果树. 2024(05): 20-25 .
9.	汪梦诗，祁雅楠，赵沁雨，兰天，鲍诗晗，孙翔宇，马婷婷. 五种陕西主栽猕猴桃品种营养品质与香气特征解析. 食品工业科技. 2024(23): 272-281 .
10.	贺迪，钟彩虹，朱佳慧，潘慧，李文艺，杨洁，黄跃，刘普，李黎. 山梨与中华猕猴桃种间杂交群体的抗病性评价及抗病机制的研究. 果树学报. 2024(11): 2235-2249 .
11.	唐玉凤，朱世银，蔡荣靖，胡志芳，田虹，张小龙，王世敏，蒙元燕，全勇. 威信县5个主要猕猴桃品种的果实品质比较. 云南农业科技. 2024(05): 1-5 .
12.	公旭晨，毛积鹏，高磊，林孟飞，卢玉鹏，王小玲，高柱. 6个猕猴桃品种果实发育期品质变化规律分析. 中国南方果树. 2024(06): 216-224+232 .

Other cited types(6)

Get Citation

PDF

XML

Article views (92) PDF downloads (7) Cited by(18)

Turn off MathJax

Article Contents

Abstract

References

Assessing microbial diversity in anthers of Eriobotrya japonica (Thunb.) Lindl. based on high-throughput sequencing