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Growth and physiological responses of selected pakchoi varieties to Plasmodiophora brassicae infection

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Abstract

Clubroot disease, caused by Plasmodiophora brassicae, is a serious soil-borne disease of Brassica crops worldwide. Pakchoi is one of the most important cruciferous vegetable crops and commonly infected by P. brassicae. To date, the physiological changes and mechanism of pakchoi in response to P. brassicae are largely unknown. In this study, seedlings of two pakchoi cultivars, cv. Xinxiaqing (a clubroot-susceptible cultivar) and Yanlong (a less susceptible cultivar than Xinxiaqing), were inoculated with P. brassicae. Results showed that infected roots were enlarged and changed into club shape galls. Fresh root weight, relative electrical conductivity, the activity of lactate dehydrogenase (LDH) and alcohol dehydrogenase (ADH) in infected roots were significantly induced. In contrast, a significant reduction of root length, root function, and the activity of succinic dehydrogenase (SDH), catalase (CAT), ascorbate peroxidase (APX), and superoxide dismutase (SOD) were observed in diseased roots. Interestingly, activities of malate dehydrogenase (MDH) and peroxidase (POD) in S1 and S2 plant roots were increased and decreased in S3 plant roots. Additionally, infected Xinxiaqing roots showed more serious disease symptoms than Yanlong, and the antioxidant enzyme activities were lowered in Xinxiaqing roots compared with those in infected Yanlong roots, indicating the importance of these enzymes in plant resistance against clubroot disease.

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References

  • Amthor JS (1984) The role of maintenance respiration in plant growth. Plant Cell Environ 8:561–569

    Google Scholar 

  • Balamuralikrishnan M, Doraisamy S, Ganapathy T, Viswanathan R (2005) Effects of biotic and abiotic agents on sugarcane mosaic virus titre. Oxidative Enzymes and Phenolics in Sorghum bicolor. Acta Phytopathol Entomol Hung 40(1):9–22

    Article  CAS  Google Scholar 

  • Benz A, Spring O (1995) Identification and characterization of an auxin-degrading enzyme in downy mildew infected sunflower. Physiol Mol Plant Pathol 3:163–175

    Article  Google Scholar 

  • Biemelt S, Albrecht G (1998) Re-aeration following hypoxia or anoxia leads to activation of the antioxidative defense system in roots of wheat seedlings. Plant Physiol 2:651–658

    Article  Google Scholar 

  • Bourgeron T, Rustin P, Chretien D, Birch-Machin M, Bourgeois M, Viegas-Péquignot E, Munnich A, Rötig A (1995) Mutation of a nuclear succinate dehydrogenase gene results in mitochondrial respiratory chain deficiency. Nat Genet 2:144–149

    Article  Google Scholar 

  • Chen J, Pang W, Bing C, Zhang C, Piao Z (2016) Transcriptome analysis of Brassica rapa near-isogenic lines carrying Clubroot-resistant and –susceptible alleles in response to Plasmodiophora brassicae during early infection. Front Plant Sci 1183

  • Cooley JW, Vermaas WFJ (2001) Succinate dehydrogenase and other respiratory pathways in thylakoid membranes of Synechocystis sp. strain PCC 6803: capacity comparisons and physiological function. J Bacteriol 14:4251–4258

    Article  Google Scholar 

  • Ding GQ (2016) Prevention and control technology of clubroot in cruciferous vegetables in Shanghai. Shanghai Vegetables. 6:31–32

  • Donald C, Porter I, Dixon GR (2009) Integrated control of clubroot. J Plant Growth Regul 3:289–303

    Article  Google Scholar 

  • Durner J, Klessig DF (1996) Salicylic acid is a modulator of tobacco and mammalian catalases. J Biol Chem 45:28492–28501

    Article  Google Scholar 

  • Friberg H, Lagerlöf J, Rämert B (2005) Germination of Plasmodiophora brassicae resting spores stimulated by a non-host plant. Eur J Plant Pathol 3:275

    Article  Google Scholar 

  • Guo XX, LI XX, Zhu HF, Zhu YY, Hou RX, Hou XL (2015) Respiratory metabolism of Pakchoi seedlings roots under water logging stress. Acta Bot Boreal-Occid Sin 35(4):0793–0800

  • Hammerschmidt R, Nuckles EM, Kuć J (1982) Association of enhanced peroxidase activity with induced systemic resistance of cucumber to Colletotrichum lagenarium ☆. Physiol Plant Pathol 1:73–76

    Article  Google Scholar 

  • Hao Z, Wang L, He Y, Liang J, Tao R (2011) Expression of defense genes and activities of antioxidant enzymes in rice resistance to rice stripe virus and small brown planthopper. Plant Physiol Bioch 49(7):744–751

    Article  CAS  Google Scholar 

  • Hawker JS (1969) Changes in the activities of malic enzyme, malate dehydrogenase, phosphopyruvate carboxylase during the development of a non-climacteric fruit (the grape). Phytochemistry 8:19–23

    Article  CAS  Google Scholar 

  • He L, Li B, Lu X, Yuan L, Yang Y, Yuan Y, Du J, Guo S (2015) The effect of exogenous calcium on mitochondria, respiratory metabolism enzymes and ion transport in cucumber roots under hypoxia. Sci Rep 11391:11391

    Article  Google Scholar 

  • Hou XL (2003) Advances in breeding of non-heading Chinese cabbage. Journal of Nanjing Agricultural University 26(4):111–115

  • Huang R, Huang RH, Hua JL, Liang YY, Shao JY (2012) Study on inoculation methods and condition of Clubroot in Brassica rapa chinensis. Chinese Agricultural Science Bulletin 28(31):252–255

  • Hwang SF, Strelkov SE, Feng J, Gossen BD, Howard RJ (2012) Plasmodiophora brassicae: a review of an emerging pathogen of the Canadian canola (Brassica napus) crop. Mol Plant Pathol 2:105

    Article  Google Scholar 

  • Ingram DS, Tommerup IC (1972) The life history of Plasmodiophora brassicae Woron. Roy Soc London Proc Ser B Biol Sci 1058:103–112

    Google Scholar 

  • Ishikawa T, Okazaki K, Nagaoka T, Itoh K, Mitsui T, Hori H (2010) Isoform-specific localization of Brassica rapa Nitrilases in root infected with Plasmodiophora brassicae revealed using in situ hybridization probes improved with locked nucleic acids. J Plant Growth Regul 2:210–222

    Article  Google Scholar 

  • Jian Z, Tian XL, Qiao LF, Pei Q (2012) Respiratory enzyme activity and regulation of respiration pathway in seashore mallow (Kosteletzkya virginica) seedlings under waterlogging conditions. Aust J Crop Sci 4

  • Li J, Hu XH, Guo SR, Jia YX, Du CX (2007) Effects of D-arginine on polyamine content and anaerobic respiration metabolism of cucumber seedling roots under hypoxia stress. Ying Yong Sheng Tai Xue Bao 2:376–382

    Google Scholar 

  • Li Y, Dash RK, Kim J, Saidel GM, Cabrera ME (2009) Role of NADH/NAD+ transport activity and glycogen store on skeletal muscle energy metabolism during exercise: in silico studies. Am J Physiol Cell Physiol 1:25–46

    Article  Google Scholar 

  • Liu TJ, Zheng XG, Li JS, Wang LP, Chen GM, Han XY, Ju L (2009) Effects of waterlogging stress on roots physiological and biochemical characteristics and growth of grafted red-seed edible seed watermelon seedlings. Journal of Changjiang Vegetables 2b,18–21

  • Lu XX, Kang XH. , Fu JM, Lv XJ , Wang MH. (2013). Effect of rape plasmodiophora brassicae on photosynthesis and enzymatic activity of rape. Guangdong Agricultural Sciences, 40(24), 71–70

  • Lücke T, Höppner W, Schmidt E, Illsinger S, Das AM (2004) Fabry disease: reduced activities of respiratory chain enzymes with decreased levels of energy-rich phosphates in fibroblasts. Mol Genet Metab 1:93–97

    Article  Google Scholar 

  • Luo HH, Zhang YL, Zhang WF (2016) Effects of water stress and rewatering on photosynthesis, root activity, and yield of cotton with drip irrigation under mulch. Photosynthetica. 1:65–73

    Article  Google Scholar 

  • Mei Y, Ding G, Lei S, Ji F, Xu F, Meng J (2010) Quantitative trait loci for root morphology in response to low phosphorus stress in Brassica napus. Theor Appl Genet 1:181

    Google Scholar 

  • Mithen R, Magrath R (1992) A contribution to the life history of Plasmodiophora brassicae: secondary plasmodia development in root galls of Arabidopsis thaliana. Mycol Res 10:877–885

    Article  Google Scholar 

  • Murshed R, Lopez-Lauri F, Sallanon H (2014) Effect of water stress on antioxidant systems and oxidative parameters in fruits of tomato (Solanum lycopersicon L, cv. Micro-tom). Physiol Mol Biol Plants 19(3):363–378

    Article  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by Ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 5:867–880

    Google Scholar 

  • Qin SJ., Lv DG., Li ZX, Ma HY., Liu LZ., Liu, GC (2011) Effects of water stress on respiration and other physiological metabolisms of Cerasus sachalinensis Kom. Seedlings. Scientia Agricultura Sinica 44(1):201–209

  • Ramakrishna B, Rao SSR (2012) 24-Epibrassinolide alleviated zinc-induced oxidative stress in radish (Raphanus sativus L.) seedlings by enhancing antioxidative system. Plant Growth Regul 2:249–259

    Article  Google Scholar 

  • Shang S, Huang MJ, Tian LB (2009) Progress of studies on biological characters and molecular biology of Club root disease on cruciferous crops. Journal of Jilin Agricultural Sciences 34(2):43–46

  • Siemens J, Nagel M, Ludwig-Müller J, Sacristán MD (2002) The interaction of Plasmodiophora brassicae and Arabidopsis thaliana : parameters for disease quantification and screening of mutant lines. J Phytopathol 11-12:592–605

    Article  Google Scholar 

  • Suwabe K, Tsukazaki H, Iketani H, Hatakeyama K, Fujimura M, Nunome T, Fukuoka H, Matsumoto S, Hirai M (2003) Identification of two loci for resistance to Clubroot (Plasmodiophora Brassicae Woronin) in Brassica Rapa L. Theor Appl Genet 107:997–1002

    Article  CAS  Google Scholar 

  • Tao C, Kai B, He Z, Gao Z, Ying Z, Fu Y, Cheng J, Xie J, Jiang D (2016) Arabidopsis mutant bik1 exhibits strong resistance to Plasmodiophora brassicae. Front Physiol 539

  • Tomaz T, Bagard M, Pracharoenwattana I, Lindén P, Lee CP, Carroll AJ, Ströher E, Smith SM, Gardeström P, Millar AH (2010) Mitochondrial malate dehydrogenase lowers leaf respiration and supports photorespiratory carbon flux and plant growth in Arabidopsis. Plant Physiol 3:1143–1157

    Article  Google Scholar 

  • Toxopeus H, Janssen AMP (1975) Clubroot resistance in turnip II. The ‘slurry’ screening method and clubroot races in the Netherlands. Euphytica. 3:751–755

    Article  Google Scholar 

  • Wu XX, He J, Ding HD, Zhu ZW, Chen JL, Xu S, Zha DS (2015) Modulation of zinc-induced oxidative damage in solanum melongena by 6-benzylaminopurine involves ascorbate–glutathione cycle metabolism. Environ Exp Bot 116:1–11

    Article  CAS  Google Scholar 

  • Zhang ER, Ren YY, Hu HQ, Liu YH, Chen SS (2009) Effects of calcium on growth and respiratory metabolism of hot pepper seedling roots under flood stress. Acta Horticulturae Sinica 36(12):1749–1754

  • Zhang X, Huang G, Bian X, Zhao Q (2013) Effects of root interaction and nitrogen fertilization on the chlorophyll content, root activity, photosynthetic characteristics of intercropped soybean and microbial quantity in the rhizosphere. Plant Soil Environ 2:80–88

    Article  Google Scholar 

  • Zhu HF, Li Xf, Zhu YY, Guo XX, Liu JP, Gao QQ, Zhai W (2015) Effects of Clubroot disease on growth, physiochemical substance and reactive oxygen metabolism in Pak-choi. Acta Botanica Boreali-Occidentalia Sinica 35(12):2469-2476

Download references

Acknowledgments

This work was supported by Agriculture Research System of Shanghai, China (Grant No. 201903) and National Key R&D Program of China 2017YFD0101803. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Author notes

  1. Hongfang Zhu and Xiaofeng Li contributed equally to this work.

Authors and Affiliations

  1. Shanghai Key Lab of Protected Horticultural Technology, Horticulture Research Institute, Shanghai Academy of Agriculture Sciences, Shanghai, China

    Hongfang Zhu, Xiaofeng Li, Dandan Xi, Zhaohui Zhang & Yuying Zhu

  2. Key Laboratory of Urban Agriculture, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, 200240, China

    Muhammad Khalid

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  1. Hongfang Zhu
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  2. Xiaofeng Li
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  3. Muhammad Khalid
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Correspondence to Yuying Zhu.

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Zhu, H., Li, X., Khalid, M. et al. Growth and physiological responses of selected pakchoi varieties to Plasmodiophora brassicae infection. J Plant Pathol 102, 459–467 (2020). https://doi.org/10.1007/s42161-019-00470-9

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