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Journal of Integrative Agriculture  2024, Vol. 23 Issue (9): 3025-3044    DOI: 10.1016/j.jia.2024.07.011
Special Issue: 园艺作物品质提升与逆境适应性Horticulture——Quality Improvement & Stress adaptation
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Dopamine improves apple replant disease resistance by regulating physiological resilience and rhizosphere microbial community structure

Peihua Du*, Yang Cao*, Huaite Liu, Jiahao Ji, Wei Sun, Xueying Zhang, Jizhong Xu, Bowen Liang#

College of Horticulture, Hebei Agricultural University, Baoding 071001, China
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摘要  

多种胁迫因素诱发的苹果再植病是一种复杂的农业问题,会升高植株的活性氧水平,并且限制养分利用。然而,现有的对策难以有效应对这一挑战。本研究中,我们以平邑甜茶为实验材料,利用盆栽实验方式来研究多巴胺缓解ARD的能力。外源施用100 μmol L-1多巴胺显著促进了再植土中苹果的生长,相对生长速率提高17.44%。我们的研究结果揭示了多巴胺调节苹果ARD抗性的两条主要途径。首先,多巴胺有效降低ROS水平,激活氮转运和代谢相关基因的表达。其中,MdNPL5、MdNRT1.1、MdNPL2、MdNRT2.5、MdNPL3、MdNRT2.4、MdNADH-GAGOT和MdFd-GAGOT受多巴胺强烈调控。这些调控作用促进了苹果植株对土壤氮的吸收和利用。其次,多巴胺改善了土壤理化性质,增强了微生物群落多样性,促进了微生物群落之间的相互协作关系。此外,多巴胺还改变了根际土壤微生物的结构 (上调: Clostridiales, Gaiellales, Sordariales和Mortierellales; 下调:Micrococcales, Longimicrobium, Hypocreales 和 Cystobasidiales)。值得注意的是,多巴胺显著上调了Gaiella和 Mortierella的丰度。这两种菌属的丰度与土壤脲酶活性、土壤有效氮含量、植物生长和氮吸收均呈显著正相关关系。多巴胺还显著降低了再植土壤中植物病原菌Gibberella的丰度(11.71倍)。我们的研究结果揭示了多巴胺促进ARD抗性的机制,将有助于苹果产业的可持续发展。



Abstract  
Apple replant disease (ARD) is a complex agricultural problem caused by multiple stressors that can lead to increased reactive oxygen species (ROS) levels and limited nutrient utilization in plants.  However, existing countermeasures cannot effectively address this challenge.  Here, we used Malus hupehensis as a test organism to investigate whether the pleiotropic molecule dopamine can alleviate ARD using pot experiments.  Exogenous application of 100 μmol L–1 dopamine significantly promoted the growth of apple seedlings in the replanted soil, with a relative growth rate increase of 17.44%.  Our results revealed two major pathways by which dopamine regulates ARD resistance in apple trees.  First, dopamine effectively reduces the level of ROS and activates the expression of genes related to nitrogen (N) transport and metabolism.  Among those genes, MdNLP5, MdNRT1.1, MdNLP2, MdNRT2.5, MdNLP3, MdNRT2.4, MdNADH-GAGOT, and MdFd-GAGOT were strongly regulated by dopamine.  These regulatory effects promoted the uptake and utilization of soil N by the plants.  Second, dopamine improved the physical and chemical properties, enhanced microbial community diversity, and promoted mutual cooperation between microbial communities in the soil.  Furthermore, dopamine altered the microbial structure of rhizosphere soil (upregulating Clostridiales, Gaiellales, Sordariales and Mortierellales; downregulating Micrococcales, Longimicrobiales, Hypocreales and Cystobasidiales).  Notably, dopamine significantly upregulated the abundances of Gaiella and Mortierella, both of which were positively correlated with soil urease activity, soil available N content, plant growth and N uptake.  Dopamine also significantly downregulated the abundance of the plant pathogen Gibberella (by 11.71-fold) in replant soil.  Our results provide insights into the mechanisms by which dopamine promotes ARD resistance, and can promote the sustainable development of the apple industry.


Keywords:  continuous cropping barrier       exogenous dopamine        Malus hupehensis Rehd        15N-labeling        soil microbiome  
Received: 13 January 2023   Accepted: 02 April 2024
Fund: 
This work was supported by National Natural Science Foundation of China (31901964), the Science and Technology Project of Hebei Education Department, China (BJK2022012), the Innovation Ability Training Project for Graduate Student of Hebei Province, China (CXZZBS2023071), the Introduced Talents Project of Hebei Agricultural University, China (YJ201904), the Key Research and Development Project of Hebei Province, China (21326308D-02-03) and the Earmarked Fund for the China Agricultural Research System, China (CARS-27).
About author:  #Correspondence Bowen Liang, E-mail: lbwnwsuaf@126.com, lbw@hebau.edu.cn *These authors contributed equally to this study.

Cite this article: 

Peihua Du, Yang Cao, Huaite Liu, Jiahao Ji, Wei Sun, Xueying Zhang, Jizhong Xu, Bowen Liang. 2024. Dopamine improves apple replant disease resistance by regulating physiological resilience and rhizosphere microbial community structure. Journal of Integrative Agriculture, 23(9): 3025-3044.

Ahmad A, Khan W U, Shah A A, Yasin N A, Ali A, Rizwan M, Ali S. 2021. Dopamine alleviates hydrocarbon stress in Brassica oleracea through modulation of physio-biochemical attributes and antioxidant defense systems. Chemosphere, 270, 128633.

Albuquerque L, Franca L, Rainey F A, Schumann P, Nobre M F, da Costa M S. 2011. Gaiella occulta gen. nov., sp nov., a novel representative of a deep branching phylogenetic lineage within the class Actinobacteria and proposal of Gaiellaceae fam. nov and Gaiellales ord. nov. Systematic and Applied Microbiology, 34, 595–599.

An M J, Chang D D, Hong D S, Fan H, Wang K Y. 2021. Metabolic regulation in soil microbial succession and niche differentiation by the polymer amendment under cadmium stress. Journal of Hazardous Materials, 416, 126094.

Berg G, Smalla K. 2009. Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiology Ecology, 68, 1–13.

Cavael U, Diehl K, Lentzsch P. 2020. Assessment of growth suppression in apple production with replant soils. Ecological Indicators, 109, 105046.

Chen S M, Waghmode T R, Sun R B, Kuramae E E, Hu C S, Liu B B. 2019. Root-associated microbiomes of wheat under the combined effect of plant development and nitrogen fertilization. Microbiome, 7, 136.

Chen Z, Maltz M R, Zhang Y G, O’Brien B J, Neff M, Wang Y H, Cao J X. 2021. Plantations of Cinnamomum camphora (Linn) Presl with distinct soil bacterial communities mitigate soil acidity within polluted locations in southwest China. Forests, 12, 657.

Chen Z, Ren W, Yi X, Li Q, Cai H G, Farhan A, Yuan L X, Mi G H, Pan Q C, Chen F J. 2023. Local nitrogen application increases maize post-silking nitrogen uptake of responsive genotypes via enhanced deep root growth. Journal of Integrative Agriculture, 22, 235–250.

Deng X H, Zhang N, Li Y C, Zhu C Z, Qu B Y, Liu H J, Li R, Bai Y, Shen Q R, Salles J F. 2022. Bio-organic soil amendment promotes the suppression of Ralstonia solanacearum by inducing changes in the functionality and composition of rhizosphere bacterial communities. New Phytologist, 235, 1558–1574.

Du P H, Yin B Y, Cao Y, Han R X, Ji J H, He X L, Liang B W, Xu J Z. 2022a. Beneficial effects of exogenous melatonin and dopamine on low nitrate stress in Malus hupehensis. Frontiers in Plant Science, 12, 807472.

Du P H, Yin B Y, Zhou S S, Li Z Y, Zhang X Y, Cao Y, Han R X, Shi C J, Liang B W, Xu J Z. 2022b. Melatonin and dopamine mediate the regulation of nitrogen uptake and metabolism at low ammonium levels in Malus hupehensis. Plant Physiology and Biochemistry, 171, 182–190.

Gao M, Zhou J J, Wang E T, Chen Q, Xu J, Sun J G. 2015. Multiphasic characterization of a plant growth promoting bacterial strain, Burkholderia sp. 7016 and its effect on tomato growth in the field. Journal of Integrative Agriculture, 14, 1855–1863.

Gao T T, Liu X M, Shan L, Wu Q, Liu Y, Zhang Z J, Ma F W, Li C. 2020. Dopamine and arbuscular mycorrhizal fungi act synergistically to promote apple growth under salt stress. Environmental and Experimental Botany, 178, 104159.

Gao T T, Liu Y S, Liu X M, Zhao K, Shan L, Wu Q, Liu Y, Zhang Z J, Ma F W, Li C. 2021. Exogenous dopamine and overexpression of the dopamine synthase gene MdTYDC alleviated apple replant disease. Tree Physiology, 41, 1524–1541.

Gaudinier A, Rodriguez-Medina J, Zhang L F, Olson A, Liseron-Monfils C, Bagman A M, Foret J, Abbitt S, Tang M, Li B H, Runcie D E, Kliebenstein D J, Shen B, Frank M J, Ware D, Brady S M. 2018. Transcriptional regulation of nitrogen-associated metabolism and growth. Nature, 563, 259–264.

Grunewaldt-Stocker G, Mahnkopp F, Popp C, Maiss E, Winkelmann T. 2019. Diagnosis of apple replant disease (ARD): Microscopic evidence of early symptoms in fine roots of different apple rootstock genotypes. Scientia Horticulturae, 243, 583–594.

Hu B, Jiang Z M, Wang W, Qiu Y H, Zhang Z H, Liu Y Q, Li A F, Gao X K, Liu L C, Qian Y W. 2019. Nitrate-NRT1.1B-SPX4 cascade integrates nitrogen and phosphorus signalling networks in plants. Nature Plants, 5, 401–413.

Hu L Y, Yue H, Zhang J Y, Li Y T S, Gong X Q, Zhou K, Ma F W. 2022. Overexpression of MdMIPS1 enhances drought tolerance and water-use efficiency in apple. Journal of Integrative Agriculture, 21, 1968–1981.

Jiang W T, Chen R, Zhao L, Qin L, Fan H, Chen X S, Wang Y F, Yin C M, Mao Z Q. 2022. Chemical fumigants control apple replant disease: Microbial community structure-mediated inhibition of Fusarium and degradation of phenolic acids. Journal of Hazardous Materials, 440, 129786.

Lee S M, Kong H G, Song G C, Ryu C M. 2021. Disruption of Firmicutes and Actinobacteria abundance in tomato rhizosphere causes the incidence of bacterial wilt disease. ISME Journal, 15, 330–347.

Li C, Zhao Q, Gao T T, Wang H Y, Zhang Z J, Liang B W, Wei Z W, Liu C H, Ma F W. 2018. The mitigation effects of exogenous melatonin on replant disease in apple. Journal of Pineal Research, 65, e12523.

Li F, Chen L, Redmile-Gordon M, Zhang J B, Zhang C Z, Ning Q, Li W. 2018. Mortierella elongata’s roles in organic agriculture and crop growth promotion in a mineral soil. Land Degradation & Development, 29, 1642–1651.

Liang B W, Ma C Q, Zhang Z J, Wei Z W, Gao T T, Zhao Q, Ma F W, Li C. 2018. Long-term exogenous application of melatonin improves nutrient uptake fluxes in apple plants under moderate drought stress. Environmental and Experimental Botany, 155, 650–661.

Liu X M, Gao T T, Zhang Z J, Tan K X, Jin Y B, Zhao Y J, Ma F W, Li C. 2021. The mitigation effects of exogenous dopamine on low nitrogen stress in Malus hupehensis. Journal of Integrative Agriculture, 20, 2709–2724.

Liu Y, von Wiren N. 2017. Ammonium as a signal for physiological and morphological responses in plants. Journal of Experimental Botany, 68, 2581–2592.

Lucas M, Balbin-Suarez A, Smalla K, Vetterlein D. 2018. Root growth, function and rhizosphere microbiome analyses show local rather than systemic effects in apple plant response to replant disease soil. PLoS ONE, 13, e0204922.

O’Brien J A, Vega A, Bouguyon E, Krouk G, Gojon A, Coruzzi G, Gutierrez R A. 2016. Nitrate transport, sensing, and responses in plants. Molecular Plant, 9, 837–856.

Ozimek E, Hanaka A. 2021. Mortierella species as the plant growth-promoting fungi present in the agricultural soils. Agriculture-Basel, 11, 7.

Pan L H, Zhao L, Jiang W T, Wang M, Chen X S, Shen X, Yin C M, Mao Z Q. 2022. Effect of zinc oxide nanoparticles on the growth of Malus hupehensis Rehd. seedlings. Frontiers in Environmental Science, 10, 835194.

Reim S, Rohr A D, Winkelmann T, Weiss S, Liu B Y, Beerhues L, Schmitz M, Hanke M V, Flachowsky H. 2021. Genes involved in stress response and especially in phytoalexin biosynthesis are upregulated in four Malus genotypes in response to apple replant disease. Frontiers in Plant Science, 10, 1724.

Rohr A D, Staudt J, Cziborra K, Fritz A, Schmitz M, Winkelmann T. 2021. Split-root approach reveals localized root responses towards apple replant disease (ARD) in terms of ARD biomarker gene expression and content of phenolic compounds. Scientia Horticulturae, 286, 110117.

Severino R, Froufe H J C, Barroso C, Albuquerque L, Lobo-da-Cunha A, da Costa M S, Egas C. 2019. High-quality draft genome sequence of Gaiella occulta isolated from a 150 meter deep mineral water borehole and comparison with the genome sequences of other deep-branching lineages of the phylum Actinobacteria. Microbiologyopen, 8, e00840.

Sharma A, Wang J F, Xu D B, Tao S C, Chong S L, Yan D L, Li Z, Yuan H W, Zheng B S. 2020. Melatonin regulates the functional components of photosynthesis, antioxidant system, gene expression, and metabolic pathways to induce drought resistance in grafted Carya cathayensis plants. Science of the Total Environment, 713, 136675.

Shi G Y, Sun H Q, Calderon-Urrea A, Jia X X, Yang H Y, Su G L. 2020. Soil fungal diversity loss and appearance of specific fungal pathogenic communities associated with the consecutive replant problem (CRP) in lily. Frontiers in Microbiology, 11, 1649.

Snoeijers S S, Perez-Garcia A, Joosten M H A J, De Wit P J G M. 2000. The effect of nitrogen on disease development and gene expression in bacterial and fungal plant pathogens. European Journal of Plant Pathology, 106, 493–506.

Tan G, Liu Y J, Peng S G, Yin H Q, Meng D L, Tao J M, Gu Y B, Li J, Yang S, Xiao N W, Liu D M, Xiang X W, Zhou Z C. 2021. Soil potentials to resist continuous cropping obstacle: Three field cases. Environmental Research, 200, 111319.

Wang H Y, Zhang R, Mao Y F, Jiang W T, Chen X S, Shen X, Yin C M, Mao Z Q. 2022. Effects of Trichoderma asperellum 6S–2 on apple tree growth and replanted soil microbial environment. Journal of Fungi, 8, 63.

Wang H Y, Zhao L, Jiang W T, Zhang R, Chen R, Mao Y F, Chen X S, Shen X, Yin C M, Mao Z Q. 2021. Effects of Allium fistulosum-Brassica juncea-Triticum aestivum rotation a year on the soil microbial environment and the subsequent growth of young apple trees. Scientia Horticulturae, 290, 110549.

Wang X Q, Yao Y Y, Wang G W, Lu H, Ma J Z, Zhang M S, Chen X S, Yin C M, Mao Z Q. 2022. Controlled-Release diammonium phosphate alleviates apple replant disease: An integrated analysis of soil properties, plant growth, and the soil microbiome. Journal of Agricultural and Food Chemistry, 70, 8942–8954.

Wang Y J, Liu L, Luo Y, Awasthi M K, Yang J F, Duan Y M, Li H K, Zhao Z Y. 2020. Mulching practices alter the bacterial-fungal community and network in favor of soil quality in a semiarid orchard system. Science of the Total Environment, 725, 138527.

Wang Y Y, Cheng Y H, Chen K E, Tsay Y F. 2018. Nitrate transport, signaling, and use efficiency. Annual Review of Plant Biology, 69, 85–122.

Wu H M, Qin X J, Wang J Y, Wu L K, Chen J, Fan J K, Zheng L, Tangtai H P, Arafat Y, Lin W W, Luo X M, Lin S, Lin W X. 2019. Rhizosphere responses to environmental conditions in Radix pseudostellariae under continuous monoculture regimes. Agriculture Ecosystems & Environment, 270, 19–31.

Wu H M, Wu H M, Jiao Y Y, Zhang Z Y, Rensing C, Lin W X. 2022. The combination of biochar and PGPBs stimulates the differentiation in rhizosphere soil microbiome and metabolites to suppress soil-borne pathogens under consecutive monoculture regimes. Global Change Biology Bioenergy, 14, 84–103.

Wu H M, Wu H M, Qin X J, Lin M H, Zhao Y L, Rensing C, Lin W X. 2021. Replanting disease alters the faunal community composition and diversity in the rhizosphere soil of Radix pseudostellariae. Agriculture Ecosystems & Environment, 310, 107304.

Wu H M, Wu L K, Zhu Q, Wang J Y, Qin X J, Xu J H, Kong L F, Chen J, Lin S, Khan M U, Amjad H, Lin W X. 2017. The role of organic acids on microbial deterioration in the Radix pseudostellariae rhizosphere under continuous monoculture regimes. Scientific Reports, 7, 3497.

Xiang L, Wang M, Jiang W T, Wang Y F, Chen X S, Yin C M, Mao Z Q. 2021. Key indicators for renewal and reconstruction of perennial trees soil: Microorganisms and phloridzin. Ecotoxicology and Environmental Safety, 225, 112723.

Xu X, Jiang W T, Wang G S, Ding F X, Li Q J, Wang R L, Chen X S, Shen X, Yin C M, Mao Z Q. 2023. Analysis of soil fungal community in aged apple orchards in Luochuan County, Shaanxi Province. Agriculture-Basel, 13, 63.

Yu J Q, Gu K D, Sun C H, Zhang Q Y, Wang J H, Ma F F, You C X, Hu D G, Hao Y J. 2021. The apple bHLH transcription factor MdbHLH3 functions in determining the fruit carbohydrates and malate. Plant Biotechnology Journal, 19, 285–299.

Zhang B, Fan W M, Zhu Z Z, Wang Y, Zhao Z Y. 2023. Functional analysis of MdSUT2.1, a plasma membrane sucrose transporter from apple. Journal of Integrative Agriculture, 22, 762–775.

Zhao F Y, Zhang Y Y, Dong W G, Zhang Y Q, Zhang G X, Sun Z P, Yang L J. 2019. Vermicompost can suppress Fusarium oxysporum f. sp. lycopersici via generation of beneficial bacteria in a long-term tomato monoculture soil. Plant and Soil, 440, 491–505.

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