Light stress elicits soilborne disease suppression mediated by root-secreted flavonoids in Panax notoginseng

Haiyan Fang , Cunwu Guo , Xinyue Mei , Minwen Hao , Jiayin Zhang , Lifen Luo , Haijiao Liu , Yixiang Liu , Huichuan Huang , Xiahong He , Youyong Zhu , Min Yang , Shusheng Zhu

Horticulture Research ›› 2024, Vol. 11 ›› Issue (10) : 213

PDF (198KB)
Horticulture Research ›› 2024, Vol. 11 ›› Issue (10) :213 DOI: 10.1093/hr/uhae213
Articles
research-article
Light stress elicits soilborne disease suppression mediated by root-secreted flavonoids in Panax notoginseng
Author information +
History +
PDF (198KB)

Abstract

Developing disease-suppressive soils is an effective approach for managing soilborne diseases, which can be achieved through crop metabolism and root secretion modification to recruit beneficial soil microbiota. Many factors, such as light, can elicit and modify plant metabolomic activities, resulting in disease suppression. To investigate the impact of light, Panax notoginseng was planted in a greenhouse and forest, conditioned with three levels of light intensities, including the optimal (15% light transmittance of full light), suboptimal low (5% light transmittance of full light) and suboptimal high (30% light transmittance of full light) intensities. We assessed the rhizosphere microbiota of P. notoginseng and root rot disease caused by soilborne pathogen Ilyonectria destructans, and elucidated the mechanism. Results showed that suboptimal light conditions alleviated root rot disease of P. notoginseng by enriching beneficial microbiota in the rhizosphere. Both low and high light stresses enhanced the secondary metabolism profile in favor of plant defense, particularly the flavonoid pathway. Notably, high light stress demonstrated a robust ability to promote flavonoid metabolism and secretion, resulting in the enrichment of more beneficial microorganisms that suppressed the soilborne pathogen I. destructans. These findings highlight the potential for adjusting canopy light intensities to improve soil health and promote sustainable agriculture.

Cite this article

Download citation ▾
Haiyan Fang, Cunwu Guo, Xinyue Mei, Minwen Hao, Jiayin Zhang, Lifen Luo, Haijiao Liu, Yixiang Liu, Huichuan Huang, Xiahong He, Youyong Zhu, Min Yang, Shusheng Zhu. Light stress elicits soilborne disease suppression mediated by root-secreted flavonoids in Panax notoginseng. Horticulture Research, 2024, 11 (10) : 213 DOI:10.1093/hr/uhae213

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgements

This study was financially supported by the Natural Science Foundation of China (U23A20202), the Major Science and Technology Project in Yunnan Province (202102AE090042), and the Major Science and Technology Project of Kunming (2021JH002).

Author contributions

H.F., C.G., and S.Z. conducted all experiments, conceived the study, and prepared the manuscript; S.Z., M.Y., and Y.Z. conceived the study, and supervised the project; X.M., Y.L., H.H., X.H., L.L., and H.L. provided critical comments on the study, and helped in manuscript revision; M.H. and J.Z. assisted in the study.

Data availability

The data supporting the findings of this study are available within the paper and its supplementary information files. The raw sequencing reads were deposited in the NCBI Sequence Read Archive (SRA) database. The underforest fungi and bacteria are denoted by PRJNA1074228 and RJNA1074125, respectively. The glasshouse fungi and bacteria are denoted by PRJNA1074256 and PRJNA1074252, respectively.

Conflict of interest

None declared.

Supplementary data

Supplementary data are available at Horticulture Research online.

References

[1]

Chen XX, Yu HD, Li MQ. et al. Research status and trends of root rot disease based on bibliometric analysis. Chinese J Appl Environ Biol. 2024; 30:623-32

[2]

Arora H, Sharma A, Sharma S. et al. Pythium damping-off and root rot of Capsicum annuum L.: impacts, diagnosis, and management. Microorganisms. 2021; 9:823

[3]

Bischoff Nunes I, Goodwin PH. Interaction of ginseng with Ilyonectria root rot pathogens. Plants (Basel). 2022; 11:2152

[4]

Yang M, Yaun Y, Huang H. et al. Steaming combined with biochar application eliminates negative plant-soil feedback for sanqi cultivation. Soil Tillage Res. 2019; 189:189-98

[5]

Sun J, Li S, Fan C. et al. N-Acetylglucosamine promotes tomato plant growth by shaping the community structure and metabolism of the rhizosphere microbiome. Microbiol Spectr. 2022; 10:e0035822

[6]

Shennan C, Muramoto J, Koike S. et al. Anaerobic soil disinfestation is an alternative to soil fumigation for control of some soil-borne pathogens in strawberry production. Plant Pathol. 2017; 67:51-66

[7]

Saad MM, Eida AA, Hirt H. Tailoring plant-associated microbial inoculants in agriculture: a roadmap for successful application. J Exp Bot. 2020; 71:3878-901

[8]

Dastogeer KMG, Tumpa FH, Sultana A. et al. Plant microbiome - an account of the factors that shape community composition and diversity. Current Plant Biol. 2020; 23:100161

[9]

Raza W, Wei Z, Jousset A. et al. Extended plant metarhizobiome: understanding volatile organic compound signaling in plant-microbe metapopulation networks. mSystems. 2021; 6:e0084921

[10]

Zhalnina K, Louie KB, Hao Z. et al. Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat Microbiol. 2018; 3:470-80

[11]

Chai YN, Schachtman DP. Root exudates impact plant performance under abiotic stress. Trends Plant Sci. 2022; 27:80-91

[12]

Raaijmakers JM, Mazzola M. ECOLOGY. Soil immune responses. Science. 2016; 352:1392-3

[13]

Yuan J, Zhao J, Wen T. et al. Root exudates drive the soil-borne legacy of aboveground pathogen infection. Microbiome. 2018; 6:156

[14]

Luo L, Zhang J, Ye C. et al. Foliar pathogen infection manipulates soil health through root exudate-modified rhizosphere microbiome. Microbiol Spectr. 2022; 10:e0241822

[15]

Lee H-R, Lee S, Park S. et al. Transient expression of whitefly effectors in Nicotiana benthamiana leaves activates systemic immunity against the leaf pathogen Pseudomonas syringae and soilborne pathogen Ralstonia solanacearum. Front Ecol Evol. 2018; 6

[16]

Guo C, Yang M, Jiang B. et al. Moisture controls the suppression of Panax notoginseng root rot disease by indigenous bacterial communities. mSystems. 2022; 7:e0041822

[17]

Yu JB, Bai M, Wang C. et al. Regulation of secondary metabolites accumulation in medicinal plants by rhizospheric and endophytic microorganisms. Med. Plant Biol. 2024; 3:e011

[18]

Prescott CE, Grayston SJ, Helmisaari HS. et al. Surplus carbon drives allocation and plant-soil interactions. Trends Ecol Evol. 2020; 35:1110-8

[19]

Wen Z, White PJ, Shen J. et al. Linking root exudation to belowground economic traits for resource acquisition. New Phytol. 2022; 233:1620-35

[20]

Hou S, Wolinska KW, Hacquard S. Microbiota-root-shoot-environment axis and stress tolerance in plants. Curr Opin Plant Biol. 2021; 62:102028

[21]

Long SP, Taylor SH, Burgess SJ. et al. Into the shadows and back into sunlight: photosynthesis in fluctuating light. Annu Rev Plant Biol. 2022; 73:617-48

[22]

Yan J, Liu J, Yang S. et al. Light quality regulates plant biomass and fruit quality through a photoreceptor-dependent HY5-LHC/CYCB module in tomato. Hortic Res. 2023; 10:uhad219

[23]

Li T, Yamane H, Tao R. Preharvest long-term exposure to UV-B radiation promotes fruit ripening and modifies stage-specific anthocyanin metabolism in highbush blueberry. Hortic Res. 2021; 8:67

[24]

Hua J. Modulation of plant immunity by light, circadian rhythm, and temperature. Curr Opin Plant Biol. 2013; 16:406-13

[25]

de Wit M, Galvão VC, Fankhauser C. Light-mediated hormonal regulation of plant growth and development. Annu Rev Plant Biol. 2016; 67:513-37

[26]

Ji NH, Chen FH, Pang ZZ. Composition identification and UV-C irradiation growth inhibition effect of green shading on the greenhouse cover. Sci Total Environ. 2022; 850:158024

[27]

Huang W, Zhang SB, Liu T. Moderate photoinhibition of photosystem II significantly affects linear electron flow in the shade-demanding plant Panax notoginseng. Front Plant Sci. 2018; 9:637

[28]

Yang M, Zhang X, Xu Y. et al. Autotoxic ginsenosides in the rhizosphere contribute to the replant failure of Panax notoginseng. PLoS One. 2015; 10:e0118555

[29]

Shuan SP, Zhang JY, Cun Z. et al. Physiological and ecological response characteristics of the shade-tolerant plant Sanqi driven by light intensity. Acta Ecol Sin. 2022; 42:3596-612

[30]

Ye C, Liu Y, Zhang J. et al. α-Terpineol fumigation alleviates negative plant-soil feedbacks of Panax notoginseng via suppressing Ascomycota and enriching antagonistic bacteria. Phytopathol Res. 2021; 3:1-17

[31]

You C, Yang TJ, Zhou XG. et al. Research progress on the mechanism and mitigation measures of intensified soilborne diseases due to continuous root exudation. Acta Pedol Sin. 2024; 61:1-11

[32]

Zhang H, Yang Y, Mei X. et al. Phenolic acids released in maize rhizosphere during maize-soybean intercropping inhibit Phytophthora blight of soybean. Front Plant Sci. 2020; 11:886

[33]

Amponsah J, Tegg RS, Thangavel T. et al. Moments of weaknesses - exploiting vulnerabilities between germination and encystment in the Phytomyxea. Biol Rev Camb Philos Soc. 2021; 96:1603-15

[34]

Pieterse CM, Zamioudis C, Berendsen RL. et al. Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol. 2014; 52:347-75

[35]

Gao Y, Yang Q, Chen Q. et al. Plants attacked above-ground by leaf-mining flies change below-ground microbiota to enhance plant defense. Hortic Res. 2024; 11:uhae121

[36]

Wei W, Yang M, Liu Y. et al. Fertilizer N application rate impacts plant-soil feedback in a sanqi production system. Sci Total Environ. 2018; 633:796-807

[37]

Luo L, Guo C, Wang L. et al. Negative plant-soil feedback driven by re-assemblage of the rhizosphere microbiome with the growth of Panax notoginseng. Front Microbiol. 2019; 10:1597

[38]

Liu H, Li Y, Ge K. et al. Interactional mechanisms of Paenibacillus polymyxa SC2 and pepper (Capsicum annuum L.) suggested by transcriptomics. BMC Microbiol. 2021; 21:70

[39]

Li Ma, Meng X, S, Y. et al. Characterization of antagonistic bacteria Paenibacillus polymyxa ZYPP18 and the effects on plant growth. Plants (Basel). 2023; 12:2504

[40]

Zhao L, Islam MS, Song P. et al. Isolation and optimization of a broad-spectrum synthetic antimicrobial peptide, ap920-WI, from Arthrobacter sp. H 5 for the biological control of plant diseases. Int J Mol Sci. 2023; 24:10598

[41]

Wen T, Yuan J, He X. et al. Enrichment of beneficial cucumber rhizosphere microbes mediated by organic acid secretion. Hortic Res. 2020; 7:154

[42]

Sharma I, Kashyap S, Agarwala N. Biotic stress-induced changes in root exudation confer plant stress tolerance by altering rhizospheric microbial community. Front Plant Sci. 2023; 14:1132824

[43]

Kumar GA, Kumar S, Bhardwaj R. et al. Recent advancements in multifaceted roles of flavonoids in plant-rhizomicrobiome interactions. Front Plant Sci. 2023; 14:1297706

[44]

Xu Z, Zhou J, Ren T. et al. Salt stress decreases seedling growth and development but increases quercetin and kaempferol content in Apocynum venetum. Plant Biol (Stuttg). 2020; 22:813-21

[45]

Arikan B, Yildiztugay E, Ozfidan-Konakci C. Protective role of quercetin and kaempferol against oxidative damage and photosynthesis inhibition in wheat chloroplasts under arsenic stress. Physiol Plant. 2023; 175:e13964

[46]

Zhang F, Huang J, Guo H. et al. OsRLCK160 contributes to flavonoid accumulation and UV-B tolerance by regulating OsbZIP48 in rice. Sci China Life Sci. 2022; 65:1380-94

[47]

Peng M, Shahzad R, Gul A. et al. Differentially evolved glucosyltransferases determine natural variation of rice flavone accumulation and UV-tolerance. Nat Commun. 2017; 8:1975

[48]

Siciliano I, Amaral Carneiro G, Spadaro D. et al. Jasmonic acid, abscisic acid, and salicylic acid are involved in the phytoalexin responses of rice to Fusarium fujikuroi, a high gibberellin producer pathogen. J Agric Food Chem. 2015; 63:8134-42

[49]

Nguyen TLA, Bhattacharya D. Antimicrobial activity of quercetin: an approach to its mechanistic principle. Molecules (Basel). 2022; 27:2494

[50]

Lahari Z, van Boerdonk S, Omoboye OO. et al. Strigolactone deficiency induces jasmonate, sugar and flavonoid phytoalexin accumulation enhancing rice defense against the blast fungus Pyricularia oryzae. New Phytol. 2024; 241:827-44

[51]

Baetz U, Martinoia E. Root exudates: the hidden part of plant defense. Trends Plant Sci. 2014; 19:90-8

[52]

Yu P, He X, Baer M. et al. Plant flavones enrich rhizosphere Oxalobacteraceae to improve maize performance under nitrogen deprivation. Nature Plants. 2021; 7:481-99

[53]

He D, Singh SK, Peng L. et al. Flavonoid-attracted Aeromonas sp. from the Arabidopsis root microbiome enhances plant dehydration resistance. ISME J. 2022; 16:2622-32

[54]

Tsuchiya H. Membrane interactions of phytochemicals as their molecular mechanism applicable to the discovery of drug leads from plants. Molecules (Basel). 2015; 20:18923-66

[55]

Lopes LAA, Dos Santos Rodrigues JB, Magnani M. et al. Inhibitory effects of flavonoids on biofilm formation by Staphylococcus aureus that overexpresses efflux protein genes. Microb Pathog. 2017; 107:193-7

[56]

Elmasri WA, Zhu R, Peng W. et al. Multitargeted flavonoid inhibition of the pathogenic bacterium Staphylococcus aureus: a proteomic characterization. J Proteome Res. 2017; 16:2579-86

[57]

Fang Y, Lu Y, Zang X. et al. 3D-QSAR and docking studies of flavonoids as potent Escherichia coli inhibitors. Sci Rep. 2016; 6:23634

[58]

Wang L, Chen M, Lam PY. et al. Multifaceted roles of flavonoids mediating plant-microbe interactions. Microbiome. 2022; 10:233

[59]

Yu XQ, Yan X, Zhang MY. et al. Flavonoids repress the production of antifungal 2,4-DAPG but potentially facilitate root colonization of the rhizobacterium Pseudomonas fluorescens. Environ Microbiol. 2020; 22:5073-89

[60]

Narayanan S, Tamura PJ, Roth MR. et al. Wheat leaf lipids during heat stress: I. High day and night temperatures result in major lipid alterations. Plant Cell Environ. 2016; 39:787-803

[61]

Park YJ, Kim YJ, Park SU. et al. Lipids and volatile organic compounds in sesame seeds and their relationships with environmental temperature-induced stress. Food Res Int. 2023; 169:112831

[62]

Hernández ML, Sicardo MD, Martínez-Rivas JM. Differential contribution of endoplasmic reticulum and chloroplast ω-3 fatty acid desaturase genes to the linolenic acid content of olive (Olea europaea) fruit. Plant Cell Physiol. 2016; 57:138-51

[63]

Li Y, Qiu L, Liu X. et al. Glycerol-induced powdery mildew resistance in wheat by regulating plant fatty acid metabolism, plant hormones cross-talk, and pathogenesis-related genes. Int J Mol Sci. 2020; 21:673

[64]

Khakdan F, Govahi M, Mohebi Z. et al. Water deficit stress responses of monoterpenes and sesquiterpenes in different Iranian cultivars of basil. Physiol Plant. 2021; 173:896-910

[65]

Rosenkranz M, Chen Y, Zhu P. et al. Volatile terpenes - mediators of plant-to-plant communication. Plant J. 2021; 108:617-31

[66]

Li C, Zha W, Li W. et al. Advances in the biosynthesis of terpenoids and their ecological functions in plant resistance. Int J Mol Sci. 2023; 24:11561

[67]

Zhong Y, Xun W, Wang X. et al. Root-secreted bitter triterpene modulates the rhizosphere microbiota to improve plant fitness. Nature Plants. 2022; 8:887-96

[68]

Kong HG, Kim BK, Song GC. et al. Aboveground whitefly infestation-mediated reshaping of the root microbiota. Front Microbiol. 2016; 7:1314

[69]

Linn AI, Zeller AK, Pfündel EE. Features and applications of a field imaging chlorophyll fluorometer to measure stress in agricultural plants. Precis Agric. 2021; 22:947-63

[70]

Lu XH, Jiao XL, Hao JJ. et al. Characterization of resistance to multiple fungicides in Botrytis cinerea populations from Asian ginseng in northeastern China. Eur J Plant Pathol. 2016; 144:467-76

[71]

Gascuel O, Steel M. Neighbor-joining revealed. Mol Biol Evol. 2006; 23:1997-2000

[72]

Liu C, Zhao D, Ma W. et al. Denitrifying sulfide removal process on high-salinity wastewaters in the presence of Halomonas sp. Appl Microbiol Biotechnol. 2016; 100:1421-6

[73]

Chen S, Zhou Y, Chen Y. et al. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018; 34:i884-90

[74]

Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013; 10:996-8

[75]

Wang Q, Garrity GM, Tiedje JM. et al. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007; 73:5261-7

[76]

Segata N, Izard J, Waldron L. et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011; 12:R60

[77]

Barberán A, Bates ST, Casamayor EO. et al. Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J. 2012; 6:343-51

[78]

Luo L-F, Yang L, Yan ZX. et al. Ginsenosides in root exudates of Panax notoginseng drive the change of soil microbiota through carbon source different utilization. Plant Soil. 2020; 455:139-53

[79]

Loo CY, Corliss DA, Ganeshkumar N. Streptococcus gordonii biofilm formation: identification of genes that code for biofilm phenotypes. J Bacteriol. 2000; 182:1374-82

PDF (198KB)

130

Accesses

0

Citation

Detail

Sections
Recommended

/