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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Amthor JS (1984) The role of maintenance respiration in plant growth. Plant Cell Environ 8:561–569
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
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
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
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
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
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
Durner J, Klessig DF (1996) Salicylic acid is a modulator of tobacco and mammalian catalases. J Biol Chem 45:28492–28501
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
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
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
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
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
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
Ingram DS, Tommerup IC (1972) The life history of Plasmodiophora brassicae Woron. Roy Soc London Proc Ser B Biol Sci 1058:103–112
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
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
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
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
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
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
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
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
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by Ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 5:867–880
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
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
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
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
Toxopeus H, Janssen AMP (1975) Clubroot resistance in turnip II. The ‘slurry’ screening method and clubroot races in the Netherlands. Euphytica. 3:751–755
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
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
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
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.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare that they have no competing interest.
Research involving human participants and/or animals
This article does not contain any studies involving human participants/animals performed by any of the authors.
Informed consent
Not applicable.
Consent for publication
All authors have read and approved this version of the article, and due care has been taken to ensure the integrity of the work. Neither the entire paper nor any part of its content has been published or has been accepted elsewhere. It is not being submitted to any other journal.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42161-019-00470-9