Scientia Agricultura Sinica ›› 2024, Vol. 57 ›› Issue (18): 3601-3611.doi: 10.3864/j.issn.0578-1752.2024.18.007

• PLANT PROTECTION • Previous Articles     Next Articles

Effect of Fatty Acid Natural Product 2E, 4E-Decadienoic Acid on Tobacco Rhizosphere Microbial Communities

PENG ZhiXin1(), ZHANG XiFen1, HAN XiaoBin2(), SI GuoDong4, XU KangWen1, ZHANG ChengSheng1,3()   

  1. 1 Institute of Tobacco Research, Chinese Academy of Agricultural Sciences/National Agricultural Environmental Microbial Resource Bank (Shandong), Qingdao 266100, Shandong
    2 Guizhou Tobacco Company, Zunyi Company, Zunyi 562400, Guizhou
    3 Qingdao Agricultural Microbial Industry Technology Innovation Center, Qingdao 266100, Shandong
    4 Hailir Pesticides and Chemicals Group Co. Ltd., Qingdao 266000, Shandong
  • Received:2024-05-29 Accepted:2024-07-27 Online:2024-09-16 Published:2024-09-29
  • Contact: HAN XiaoBin, ZHANG ChengSheng

Abstract:

【Objective】 The fatty acid compound 2E, 4E-decadienoic acid (DDA) was obtained from coculture of Bacillus subtilis Tpb55 and Trichoderma asperellum HG1, which has a specific inhibitory effect on Phytophthora. The objective of this study is to evaluate the effects of DDA on tobacco black shank (caused by P. nicotianae) and on the microbial community of tobacco rhizosphere soil, and to provide a basis for the application of such natural products in the prevention and control of plant Phytophthora disease. 【Method】 To evaluate the control efficacy of DDA against tobacco black shank, a pot experiment was performed, and the DNA copies of P. nicotianae in tobacco rhizosphere soil were detected by real-time fluorescence quantitative PCR technique. The bacterial, fungal and oomycetal communities in tobacco rhizosphere soil were analyzed through Illumina Hiseq high-throughput sequencing, and the correlation between soil nutrient factors and microbial community structure was assayed based on redundancy analysis and Mantel test. 【Result】 Compared with the control treatment with 0.5% DMSO, the treatment with 1.25 g·L-1 DDA for root irrigation showed 77.06% and 84.35% decrease for black shank disease index and P. nicotianae DNA copy number, respectively. DDA treatment also significantly increased the soil pH from 6.72 to 6.82, improved the soil conductivity by 102.11%, and decreased the soil organic matter by 13.05%. DDA treatment had no significant effect on the diversity and richness of fungi and bacteria in tobacco rhizosphere soil. However, the OTU level, Shannon index, Chao1 index, and ACE index of oomycetes significantly increased, while the Simpson index significantly decreased. The PCoA results showed that DDA treatment significantly affected the structure of tobacco rhizosphere oomycete community (r=0.667, P=0.028), but had no significant effect on fungi (r=0.259, P=0.305) and bacteria (r=0.593, P=0.098). The relative abundance of gram-positive bacterial genera such as Phycicoccus and Terrabacter significantly increased in DDA treatment, while the abundance of gram-negative bacterial genera including Devosia, Bordetella and Pseudoxanthomonas significantly decreased. Some beneficial fungi such as Aspergillus, Albifimbria, Arcopilus were enriched by DDA. For oomycetes, the relative abundance of Phytophthora was significantly decreased, but that of Globisporangium increased. The Mantel test results indicated that the changes in soil physicochemical properties caused by the application of DDA had no significant impact on the rhizosphere microbial community. 【Conclusion】2E, 4E-decadienoic acid (DDA), as a novel natural fatty acid compound, can effectively prevent and control tobacco black shank, reduce the pathogen DNA copy number in tobacco rhizosphere soil, and specifically regulate the structure of oomycete community. It has the application potential in the prevention and control of crop oomycete diseases.

Key words: Trichoderma asperellum, Bacillus subtilis, tobacco black shank, coculture, 2E, 4E-decadienoic acid (DDA), rhizosphere microbial community

Fig. 1

Effects of DDA on disease index of black shank (A) and DNA copy number of P. nicotianae in tobacco rhizosphere soil (B)"

Table 1

The physicochemical properties of tobacco rhizosphere soil affected by DDA"

处理
Treatment
pH 电导率
Conductivity (μs‧cm-1)
有机质
Organic matter (g‧kg-1)
速效钾
AK
(mg‧L-1)
铵态氮
NH4+-N
(mg‧kg-1)
速效磷
AP
(mg‧kg-1)
空白土Blank soil 6.21±0.02c 395.67±4.91a 58.40±3.22c 0.246±0a 11.08±0.57b 0.093±0.01a
CK 6.72±0.03b 192.80±2.14b 75.16±2.31a 0.216±0.01b 31.98±1.06a 0.033±0b
DDA 6.82±0.03a 389.67±8.84a 65.35±0.90b 0.206±0bc 27.96±0.98a 0.042±0.01b

Table 2

Analysis of richness and diversity of bacteria, fungi and oomycetes in rhizosphere soil of different treatments"

微生物Microorganism 处理Treatment OTU Shannon Simpson Chao1 ACE
细菌
Bacteria
CK 3688±127a 4.95±0.07a 0.01±0a 864.33±11.12a 4136.31±161.26a
DDA 3908±220a 4.98±0.02a 0.01±0a 860.67±8.96a 4344.10±231.48a
真菌
Fungi
CK 992±57a 2.83±0.02a 0.10±0.02a 274.21±9.89a 1064.75±46.45a
DDA 1006±92a 2.75±0.02a 0.11±0.01a 259.82±8.86a 1081.89±92.46a
卵菌
Oomycetes
CK 22±3b 0.19±0.02b 0.88±0.08a 21.00±1.04b 24.46±6.08b
DDA 38±3a 0.59±0.03a 0.70±0.05b 40.55±3.45a 42.34±5.70a

Fig. 2

PCoA of bacterial (A), fungal (B) and oomycetal (C) community at genus level"

Fig. 3

The bacterial (A), fungal (B) and oomycetal (C) community of tobacco rhizosphere soil at phylum level"

Fig. 4

Difference analysis of tobacco rhizosphere soil bacteria (A), fungi (B) and oomycetes (C) at genus level"

Fig. 5

RDA analysis between environmental factors and tobacco rhizosphere soil bacterial (A), fungal (B) and oomycetal (C) community"

Table 3

Mantel test of soil physicochemical properties and soil microbial community structure"

指标
Index
细菌/相关系数(<BOLD>P</BOLD>值)
Bacteria/r (P value)
真菌/相关系数(<BOLD>P</BOLD>值)
Fungi /r (P value)
卵菌/相关系数(<BOLD>P</BOLD>值)
Oomycetes/r (P value)
电导率EC -0.218 (0.492) 0.576 (0.090) 0.151 (0.760)
pH -0.114 (0.740) -0.262 (0.449) 0.072 (0.884)
速效磷AP -0.312 (0.382) - 0.006 (0.982)
速效钾AK 0.042 (0.889) -0.063 (0.879) -0.209 (0.475)
铵态氮NH4+-N 0.103 (0.758) 0.199 (0.511) -0.455 (0.104)
有机碳SOC -0.358 (0.192) 0 (1) 0.276 (0.335)
[1]
KAMOUN S, FURZER O, JONES J D, JUDELSON H S, ALI G S, DALIO R J, ROY S G, SCHENA L, ZAMBOUNIS A, PANABIÈRES F, et al. The Top 10 oomycete pathogens in molecular plant pathology. Molecular Plant Pathology, 2015, 16(4): 413-434.

doi: 10.1111/mpp.12190 pmid: 25178392
[2]
PANABIERES F, ALI G S, ALLAGUI M B, DALIO R J D, GUDMESTAD N C, KUHN M, GUHA ROY S, SCHENA L, ZAMPOUNIS A. Phytophthora nicotianae diseases worldwide: New knowledge of a long-recognised pathogen. Phytopathologia Mediterranea, 2016, 55(1): 20-40.
[3]
苗建强, 蔡萌, 张灿, 李腾蛟, 刘西莉. 植物病原卵菌对重要抑制剂的抗性分子机制研究进展. 农药学学报, 2019, 21(5/6): 736-746.
MIAO J Q, CAI M, ZHANG C, LI T J, LIU X L. Molecular resistance mechanism of phytopathogenic oomycete to several important fungicides. Chinese Journal of Pesticide Science, 2019, 21(5/6): 736-746. (in Chinese)
[4]
周怡青, 肖友利. 活性天然产物靶标蛋白的鉴定. 化学学报, 2018, 76(3): 177-189.

doi: 10.6023/A17110484
ZHOU Y Q, XIAO Y L. Target identification of bioactive natural products. Acta Chimica Sinica, 2018, 76(3): 177-189. (in Chinese)

doi: 10.6023/A17110484
[5]
SPARKS T C, BRYANT R J. Impact of natural products on discovery of, and innovation in, crop protection compounds. Pest Management Science, 2022, 78(2): 399-408.
[6]
BHATTACHARYYA A, SINHA M, SINGH H, PATEL R S, GHOSH S, SARDANA K, GHOSH S, SENGUPTA S. Mechanistic insight into the antifungal effects of a fatty acid derivative against drug-resistant fungal infections. Frontiers in Microbiology, 2020, 11: 2116.

doi: 10.3389/fmicb.2020.02116 pmid: 33013771
[7]
KUMAR P, LEE J H, BEYENAL H, LEE J. Fatty acids as antibiofilm and antivirulence agents. Trends in Microbiology, 2020, 28: 753-768.

doi: S0966-842X(20)30085-8 pmid: 32359781
[8]
WON S R, HONG M J, KIM Y M, LI C Y, KIM J W, RHEE H I. Oleic acid: An efficient inhibitor of glucosyltransferase. FEBS Letters, 2007, 581(25): 4999-5002.
[9]
SCHÖNFELD P, WOJTCZAK L. Fatty acids as modulators of the cellular production of reactive oxygen species. Free Radical Biology and Medicine, 2008, 45(3): 231-241.

doi: 10.1016/j.freeradbiomed.2008.04.029 pmid: 18482593
[10]
ZHANG X, LI Q, WANG M, MA S, ZHENG Y, LI Y, ZHAO D, ZHANG C. 2E, 4E-Decadienoic acid, a novel anti-oomycete agent from coculture of Bacillus subtilis and Trichoderma asperellum. Microbiology Spectrum, 2022, 10(4): e0154222.
[11]
LI Q, LIN W, ZHANG X, WANG M, ZHENG Y, WANG X, GAO G, LI Y, ZHAO D, ZHANG C. Transcriptomics integrated with metabolomics reveal the competitive relationship between co-cultured Trichoderma asperellum HG1 and Bacillus subtilis Tpb55. Microbiological Research, 2024, 280: 127598.
[12]
HAN T, YOU C, ZHANG L, FENG C, ZHANG C, WANG J, KONG F. Biocontrol potential of antagonist Bacillus subtilis Tpb55 against tobacco black shank. BioControl, 2016, 61: 195-205.
[13]
WANG Y, LIU M, HAN X, ZHENG Y, CHAO J, ZHANG C S. Prickly ash seed kernel: A new bio-fumigation material against tobacco black shank. Agronomy, 2020, 10(6): 770.
[14]
鲍士旦. 土壤农化分析. 北京: 中国农业出版社, 2000.
BAO S D. Soil Agrochemical Analysis. Beijing: China Agriculture Press, 2000. (in Chinese)
[15]
DURAN P, THIERGART T, GARRIDO-OTER R, AGLER M, KEMEN E, SCHULZE-LEFERT P, HACQUARD S. Microbial interkingdom interactions in roots promote Arabidopsis survival. Cell, 2018, 175(4): 973-983.e14.
[16]
CHEN Y, WANG J, YANG N, WEN Z, SUN X, CHAI Y, MA Z. Wheat microbiome bacteria can reduce virulence of a plant pathogenic fungus by altering histone acetylation. Nature Communications, 2018, 9(1): 3429.
[17]
MAGOC T, SALZBERG S L. FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics, 2011, 27(21): 2957-2963.

doi: 10.1093/bioinformatics/btr507 pmid: 21903629
[18]
EDGAR R C. UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 2013, 10(10): 996-998.

doi: 10.1038/nmeth.2604 pmid: 23955772
[19]
WANG Q, GARRITY G M, TIEDJE J M, COLE J R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 2007, 73(16): 5261-5267.

doi: 10.1128/AEM.00062-07 pmid: 17586664
[20]
YANG Z, KALIAPERUMAL K, ZHANG J, LIANG Y, GUO C, ZHANG J, YANG B, LIU Y. Antifungal fatty acid derivatives against Penicillium italicum from the deep-sea fungus Aspergillus terreus SCSIO 41202. Natural Product Research, 2021, 35(22): 4394-4401.
[21]
MILLAN A F, GAMIR J, FARRAN I, LARRAYA L, VERAMENDI J. Identification of new antifungal metabolites produced by the yeast Metschnikowia pulcherrima involved in the biocontrol of postharvest plant pathogenic fungi. Postharvest Biology and Technology, 2022, 192: 111995.
[22]
WANG Y S, HUANG Y J, CHEN W C, YEN J H. Effect of carbendazim and pencycuron on soil bacterial community. Journal of Hazardous Materials, 2009, 172: 84-91.
[23]
WANG X, SONG M, WANG Y, GAO C, ZHANG Q, CHU X, FANG H, YU Y. Response of soil bacterial community to repeated applications of carbendazim. Ecotoxicology and Environmental Safety, 2012, 75: 33-39.

doi: 10.1016/j.ecoenv.2011.08.014 pmid: 21872928
[24]
崔凯. 甲基硫菌灵及其代谢物多菌灵防控黄瓜枯萎病发生的根际微生物效应[D]. 北京: 中国农业科学院, 2021.
CUI K. The effects of thiophanate-methyl and its metabolite carbendazim on the cucumber rhizosphere microbiota in the control of cucumber Fusarium wilt[D]. Beijing: Chinese Academy of Agricultural Sciences, 2021. (in Chinese)
[25]
SANG M K, KIM K D. Plant growth-promoting rhizobacteria suppressive to Phytophthora blight affect microbial activities and communities in the rhizosphere of pepper (Capsicum annuum L.) in the field. Applied Soil Ecology, 2012, 62: 88-97.
[26]
YOU C, ZHANG C, KONG F, FENG C, WANG J. Comparison of the effects of biocontrol agent Bacillus subtilis and fungicide metalaxyl- mancozeb on bacterial communities in tobacco rhizospheric soil. Ecological Engineering, 2016, 91: 119-125.
[27]
IMFELD G, VUILLEUMIER S. Measuring the effects of pesticides on bacterial communities in soil: A critical review. European Journal of Soil Biology, 2012, 49: 22-30.
[28]
BAĆMAGA M, WYSZKOWSKA J, KUCHARSKI J. Response of soil microorganisms and enzymes to the foliar application of Helicur 250 EW fungicide on Horderum vulgare L. Chemosphere, 2020, 242: 125163.
[29]
于欣茹. 棉花根际黑曲霉和棘孢木霉抗黄萎病菌蛋白的研究[D]. 南京: 南京农业大学, 2021.
YU X R. Anti-Verticillium dahliae protein of Aspergillus niger and Trichoderma aculeatus in cotton rhizosphere[D]. Nanjing: Nanjing Agricultural University, 2021. (in Chinese)
[30]
翟妮平. 土壤淡色丝孢真菌稀有物种的挖掘及有生防潜力丝孢菌的筛选[D]. 郑州: 河南农业大学, 2019.
ZHAI N P. Exploitation of rare species of soil moniliaceous Hyphomycete and screening of potential biocontrol Hyphomycete[D]. Zhengzhou: Henan Agricultural University, 2019. (in Chinese)
[31]
TRAN T T, PHAM T Q, BARBER P A, NGUYEN C M. Control of Ceratocystis manginecans causing wilt disease on Acacia mangium seedlings. Australasian Plant Pathology, 2018, 47: 579-586.
[32]
BABA T, HIROSE D, NOMA S, BAN T. Inoculation with two Oidiodendron maius strains differentially alters the morphological characteristics of fibrous and pioneer roots of Vaccinium virgatum ‘Tifblue’ cuttings. Scientia Horticulturae, 2021, 281: 109948.
[33]
李恩星. 烟株根际土壤微生态对烟草根结线虫病的响应特征研究[D]. 昆明: 云南农业大学, 2023.
LI E X. Response characteristics of rhizosphere soil microecology of tobacco plants to tobacco root-knot nematode disease[D]. Kunming: Yunnan Agricultural University, 2023. (in Chinese)
[34]
罗嘉润. 秸秆还田配施氮肥早期对水稻生长、土壤性质及土壤微生物的影响[D]. 荆州: 长江大学, 2023.
LUO J R. Effects of straw returning and nitrogen fertilizer application on rice growth, soil properties and microbial diversity in the early stage[D]. Jingzhou: Yangtze University, 2023. (in Chinese)
[35]
李伟山, 纠敏, 周冬梅, 姚壮豪, 周阳, 魏利辉. 寡雄腐霉GAQ1对辣椒疫病的防效及对辣椒的促生作用. 植物保护学报, 2022, 49(3): 956-965.
LI W S, JIU M, ZHOU D M, YAO Z H, ZHOU Y, WEI L H. Biological control and growth-promotion effects of mycoparasitic fungus Pythium oligandrum GAQ1 against Phytophthora blight in pepper. Journal of Plant Protection, 2022, 49(3): 956-965. (in Chinese)
[36]
PAUL B. Pythium periplocum, an aggressive mycoparasite of Botrytis cinerea causing the gray mould disease of grapevine. FEMS Microbiology Letters, 1999, 181: 277-280.
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