INTERFERENCE BY NON-HOST PLANT ROOTS AND ROOT EXUDATES IN THE INFECTION PROCESSES OF PHYTOPHTHORA NICOTIANAE

Yuxin YANG, He ZHANG, Yuting FANG, Ying LI, Xinyue MEI, Huichuan HUANG, Fei DU, Shusheng ZHU, Min YANG, Yixiang LIU

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Front. Agr. Sci. Eng. ›› 2021, Vol. 8 ›› Issue (3) : 447-459. DOI: 10.15302/J-FASE-2021399
RESEARCH ARTICLE
RESEARCH ARTICLE

INTERFERENCE BY NON-HOST PLANT ROOTS AND ROOT EXUDATES IN THE INFECTION PROCESSES OF PHYTOPHTHORA NICOTIANAE

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Highlights

• The roots of non-host plant interfere infection of Phytophthora nicotianae.

• Vanillin and other compounds play key roles in antimicrobial activity of fennel roots.

• ROS accumulation is the potentially mechanism involved in inhibition of antimicrobial compounds on P. nicotianae.

Abstract

Crop rotations are widely used because they can significantly reduce the incidence of pests and diseases. The interactions between non-host roots and pathogens may be key in the inhibition of soilborne pathogens in crop rotations. Interactions between fennel (Foeniculum vulgare) roots/root exudates and Phytophthora nicotianae were investigated because of the known allelopathy between fennel and tobacco (Nicotiana tabacum). The effects of the key compounds in the fennel rhizosphere on the mycelial growth and zoospore behavior of P. nicotianae were assessed. The roots of fennel attracted P. nicotianae zoospores and inhibited their motility and the germination of cystospores, with some cystospores rupturing. 4-ethylacetophenone, vanillin and N-formylpiperidine were consistently identified in the fennel rhizosphere and were found to interfere with the infection of P. nicotianae, especially vanillin. Hyphae treated with these compounds produced more abnormal branches and accumulated reactive oxygen species. These interspecific interactions between non-host roots and pathogens were found to be an important factor in the inhibition by fennel of infection by P. nicotianae.

Graphical abstract

Keywords

fennel and tobacco rotation / infection behavior / Phytophthora nicotianae / reactive oxygen species / vanillin

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Yuxin YANG, He ZHANG, Yuting FANG, Ying LI, Xinyue MEI, Huichuan HUANG, Fei DU, Shusheng ZHU, Min YANG, Yixiang LIU. INTERFERENCE BY NON-HOST PLANT ROOTS AND ROOT EXUDATES IN THE INFECTION PROCESSES OF PHYTOPHTHORA NICOTIANAE. Front. Agr. Sci. Eng., 2021, 8(3): 447‒459 https://doi.org/10.15302/J-FASE-2021399

References

[1]
Fang Y, Zhang L, Jiao Y, Liao J, Luo L, Ji S, Li J, Dai K, Zhu S, Yang M. Tobacco rotated with rapeseed for soil-borne Phytophthora pathogen biocontrol: mediated by rapeseed root exudates. Frontiers in Microbiology, 2016, 7: 894
CrossRef Pubmed Google scholar
[2]
Yang M, Zhang Y, Qi L, Mei X, Liao J, Ding X, Deng W, Fan L, He X, Vivanco J M, Li C, Zhu Y, Zhu S. Plant-plant-microbe mechanisms involved in soil-borne disease suppression on a maize and pepper intercropping system. PLoS One, 2014, 9(12): e115052
CrossRef Pubmed Google scholar
[3]
Orlikowski L B, Oszako T. The influence of nursery cultivated plants, as well as cereals, legumes and crucifers, on selected species of Phytophthora. In: Evans H, Oszako T, eds. Alien Invasive Species and International Trade. Warsaw, Poland: Forest Research Institute, 2007, 30
[4]
Yu J Q. Allelopathic suppression of Pseudomonas solanacearum infection of tomato (Lycopersicon esculentum) in a tomato-Chinese chive (Allium tuberosum) intercropping system. Journal of Chemical Ecology, 1999, 25(11): 2409–2417
CrossRef Google scholar
[5]
Hao W Y, Ren L X, Ran W, Shen Q R. Allelopathic effects of root exudates from watermelon and rice plants on Fusarium oxysporum f. sp niveum. Plant and Soil, 2010, 336(1–2): 485–497
CrossRef Google scholar
[6]
Wang G Z, Li H G, Christie P, Zhang F S, Zhang J L, Bever J D. Plant-soil feedback contributes to intercropping overyielding by reducing the negative effect of take-all on wheat and compensating the growth of faba bean. Plant and Soil, 2017, 415(1–2): 1–12
CrossRef Google scholar
[7]
Heath M C. Nonhost resistance and nonspecific plant defenses. Current Opinion in Plant Biology, 2000, 3(4): 315–319
CrossRef Pubmed Google scholar
[8]
Zhang H, Yang Y, Mei X, Li Y, Wu J, Li Y, Wang H, Huang H, Yang M, He X, Zhu S, Liu Y. Phenolic acids released in maize rhizosphere during maize-soybean intercropping inhibit Phytophthora blight of soybean. Frontiers in Plant Science, 2020, 11: 886
CrossRef Pubmed Google scholar
[9]
Jiang B B, Zhang Y, Guo C W, Yang C Z, Zhu S S, Yang M. Control effects and allelopathic mechanism of pepper and Chinese chives intercropping on pepper Phytophthora blight. Journal of Plant Protection, 2017, 44(1): 145–151 (in Chinese)
[10]
Gao X, Wu M, Xu R, Wang X, Pan R, Kim H J, Liao H. Root interactions in a maize/soybean intercropping system control soybean soil-borne disease, red crown rot. PLoS One, 2014, 9(5): e95031
CrossRef Pubmed Google scholar
[11]
Zhu S, Morel J B. Molecular mechanisms underlying microbial disease control in intercropping. Molecular Plant-Microbe Interactions, 2019, 32(1): 20–24
CrossRef Pubmed Google scholar
[12]
Zhang D Z. Studies on the effect of rotation and intercropping to growth, yield and characteristics of cured tobacco variety KRK26. Dissertation for the Master’s Degree. Changsha: Hunan Agricultural University, 2012 (in Chinese)
[13]
Dey S, Bhattacharyya S, Bhattacharyya R. Ecosystem diversity as a function of plant and soil-microbe interactions. In: Varma A, Tripathi S, Prasad R, eds. Plant Microbiome Paradigm. Springer, 2020, 93–104
[14]
Murren C J, Alt C H S, Kohler C, Sancho G. Natural variation on whole-plant form in the wild is influenced by multivariate soil nutrient characteristics: natural selection acts on root traits. American Journal of Botany, 2020, 107(2): 319–328
CrossRef Pubmed Google scholar
[15]
Villani M G, Krueger S R, Nyrop J. A case study of the impact of the soil environment on insect/pathogen interactions: scarabs in turfgrass. In: Leslie A R, ed. Handbook of Integrated Pest Management for Turf and Ornamentals. London: CRC press, 2020
[16]
Javed R, Hanif M A, Ayub M A, Rehman R. Fennel. In: Hanif M A, Nawaz H, Khan M M, Byrne H J. Medicinal Plants of South Asia. Elsevier, 2020, 241–256
[17]
Wang X W. Cultivation technology of fennel interplanting onion. Xinjiang Agricultural Science and Technology, 2010, 4: 23 (in Chinese)
[18]
Ahmed B, Biswas M, Hawladar M M, Hossain K M F, Talukder A H M M R. Intercropping of fennel with chili. Journal of Agroforestry & Environment, 2012, 6(1): 125–128
[19]
de Carvalho L M, Nunes M U C, de Oliveira I R, Leal M L S. Yield of tomato in monocrop and intercropping with aromatics plants. Horticultura Brasileira, 2009, 27(4): 458–464
[20]
Wang S N. The allelopathic mechanism of crop rotation on alleviating muskmelon continuous cropping obstacle. Dissertation for the Doctoral Degree. Shenyang: Shenyang Agricultural University, 2017 (in Chinese)
[21]
Liu H J, Fang L, Su Y W, Zhu S S, Zhang Z L, Yang M. Antimicrobial activities test and antibacterial substance identification of fennel volatiles against the growth of Panax notoginseng root rot pathogens. Journal of Southern Agriculture, 2020, 51(9): 2145–2151 (in Chinese)
[22]
Voges M J E E E, Bai Y, Schulze-Lefert P, Sattely E S. Plant-derived coumarins shape the composition of an Arabidopsis synthetic root microbiome. Proceedings of the National Academy of Sciences of the United States of America, 2019, 116(25): 12558–12565
CrossRef Pubmed Google scholar
[23]
Ling T X, Chen J, Xue Y F, Zhou H J, Zhang X F, Fu Z Y, Qin Y H, Ma J, Han Q J, Ye X F. Inhibition effect of cinnamaldehyde against Phytophthora nicotianae in vitro. Acta Tabacaria Sinica, 2017, 23(04): 70–76 (in Chinese)
[24]
Qin G, Liu J, Cao B, Li B, Tian S. Hydrogen peroxide acts on sensitive mitochondrial proteins to induce death of a fungal pathogen revealed by proteomic analysis. PLoS One, 2011, 6(7): e21945
CrossRef Pubmed Google scholar
[25]
Fu X P, Wu F Z, Wu X, Liu D. Advances in the mechanism of improving crop mineral nutrients in intercropping and relay intercropping systems. Journal of Plant Nutrition and Fertilizer, 2016, 22(2): 525–535 (in Chinese)
[26]
Sun Y, Zhou T F, Wang Y Y, Chen J B, He X H, Li C Y, Zhu Y Y. Control effect of pepper and corn intercropping on disease and its yield increasing effect. Acta Horticultural Sinica, 2006, 33(5): 995–1000 (in Chinese)
[27]
Yang M, Mei X Y, Liao J J, Ji S G, Zhang L M, Zhang D Z, Zhu S S. Antimicrobial activity of volatiles and extracts of 3 Allium crops to plant pathogenic fungi and oomycetes. Plant Protection, 2013, 39(3): 36–44 (in Chinese)
[28]
Liao J J, Liu Y X, Yang M, Zhang Y, He X H, Zhu S S. The inhibitory activity of garlic volatiles and extracts to Phytophthora capsica. Journal of Yunnan Agricultural University, 2014, 29(03): 337–346 (in Chinese)
[29]
Liu N, Zhou B, Zhao X, Lu B, Li Y, Hao J. Grafting eggplant onto tomato rootstock to suppress Verticillium dahliae infection: the effect of root exudates. HortScience, 2009, 44(7): 2058–2062
CrossRef Google scholar
[30]
Zawoznik M S, Garrido L M, Del Pero Martinez M A, Tomaro M L. Occurrence and role of vanillin in root exudates of peanut (Arachis hypogaea). Symbiosis, 2004, 36: 257–268
[31]
Badri D V, Vivanco J M. Regulation and function of root exudates. Plant, Cell & Environment, 2009, 32(6): 666–681
CrossRef Pubmed Google scholar
[32]
Rattanapitigorn P, Arakawa M, Tsuro M. Vanillin enhances the antifungal effect of plant essential oils against Botrytis cinerea. International Journal of Aromatherapy, 2006, 16(3–4): 193–198
CrossRef Google scholar
[33]
Jaimun R, Sangsuwan J. Efficacy of chitosan-coated paper incorporated with vanillin and ethylene adsorbents on the control of anthracnose and the quality of Nam Dok Mai mango fruit. Packaging Technology & Science, 2019, 32(8): 383–394
CrossRef Google scholar
[34]
Zhou X G, Wang Z L, Pan D D, Wu F Z. Effects of vanillin on cucumber (Cucumis sativus L.) seedling rhizosphere Bacillus and Pseudomonas spp. community structures. Allelopathy Journal, 2018, 43(2): 255–264
CrossRef Google scholar
[35]
Rajabi L, Courreges C, Montoya J, Aguilera R J, Primm T P. Acetophenones with selective antimycobacterial activity. Letters in Applied Microbiology, 2005, 40(3): 212–217
CrossRef Pubmed Google scholar
[36]
Keča N, Tkaczyk M, Żółciak A, Stocki M, Kalaji H M, Nowakowska J A, Oszako T. Survival of European ash seedlings treated with phosphite after infection with the Hymenoscyphus fraxineus and Phytophthora species. Forests, 2018, 9(8): 442
CrossRef Google scholar
[37]
Hartmann A, Schmid M, Tuinen D V, Berg G. Plant-driven selection of microbes. Plant and Soil, 2009, 321: 235–257
CrossRef Google scholar
[38]
Hayakawa M, Ariizumi M, Yamazaki T, Nonomura H. Chemotaxis in the zoosporic actinomycete Catenuloplanes japonicus. Actinomycetologica, 1995, 9(2): 152–163
CrossRef Google scholar
[39]
Hosseini S, Heyman F, Olsson U, Broberg A, Funck Jensen D, Karlsson M. Zoospore chemotaxis of closely related legume-root infecting Phytophthora species towards host isoflavones. Plant Pathology, 2014, 63(3): 708–714
CrossRef Google scholar
[40]
Tyler B M. Molecular basis of recognition between Phytophthora pathogens and their hosts. Annual Review of Phytopathology, 2002, 40(1): 137–167
CrossRef Pubmed Google scholar
[41]
Lehmann S, Serrano M, L’Haridon F, Tjamos S E, Metraux J P. Reactive oxygen species and plant resistance to fungal pathogens. Phytochemistry, 2015, 112: 54–62
CrossRef Pubmed Google scholar
[42]
Tanaka A, Christensen M J, Takemoto D, Park P, Scott B. Reactive oxygen species play a role in regulating a fungus-perennial ryegrass mutualistic interaction. Plant Cell, 2006, 18(4): 1052–1066
CrossRef Pubmed Google scholar

Supplementary materials

The online version of this article at https://doi.org/10.15302/J-FASE-2021399 contains supplementary material (Fig. S1).

Acknowledgements

We thank the State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan for providing the testing platform. This study was supported by the National Natural Science Foundation of China (31972328, 31601682), the Natural Science Foundation of Yunnan Province (2018FG001-046), the Major Program in Yunnan Province (202002AE320012-02-03), the key Yunnan provincial programs of Yunnan Eco-Friendly Food International Cooperation Research Center (2019ZG00901-03), the Yunnan Academician Workstation of Chinese Academy of Engineering (2018IC063), and the Program for Innovative Research Team in Science and Technology in University of Yunnan Province.

Compliance with ethics guidelines

Yuxin Yang, He Zhang, Yuting Fang, Ying Li, Xinyue Mei, Huichuan Huang, Fei Du, Shusheng Zhu, Min Yang, and Yixiang Liu declare that they have no conflicts of interest or financial conflicts to disclose. This article does not contain any studies with human or animal subjects performed by any of the authors.

RIGHTS & PERMISSIONS

The Author(s) 2021. Published by Higher Education Press. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0)
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