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Role of Cytokinins in Clubroot Disease Development
Plant Breed. Biotech. 2019;7:73-82
Published online June 1, 2019
© 2019 Korean Society of Breeding Science.

Arif Hasan Khan Robin1,2, Mohammad Rashed Hossain1,2, Hoy-Taek Kim1, Ill-Sup Nou1, Jong-In Park1,*

1Department of Horticulture, Sunchon National University, Suncheon 57922, Korea
2Department of Genetics and Plant Breeding, Bangladesh Agricultural University, Mymensing 2202, Bangladesh
Corresponding author: *Jong-In Park, jipark@scnu.ac.kr, Tel: +82-61-750-3241, Fax: +82-61-750-5389
Received May 16, 2019; Revised May 20, 2019; Accepted May 20, 2019.
This is an Open-Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract

Clubroot, caused by the obligate biotrophic protist Plasmodiophora brassicae is a devastating disease of crucifers that causes substantial economic loss worldwide. The disease is characterized by the formation of galls in the root and hypocotyl of infected plants which restricts host vascular cambium development inhibiting efficient water and nutrient uptake by the plant. The pathogen-driven interference of hormonal homeostasis, particularly of cytokinin, in the root tissue is intricately linked with induction of hypertrophy and cell divisions leading to formation of galls. Levels of cytokinins and cell division generally increase at the onset of the disease which declines at the later stages of gall formation. The genes involved cytokinin biosynthesis such as cytokinin oxidase/dehydrogenases and isopentenyl transferases shows differential expressions during clubroot infection and gall expansion in root tissues. Wider understanding of the roles of cytokinins and associated genes along the development of the disease will be helpful in unravelling plants defense mechanism against clubroot disease.

Keywords : Brassica, Clubroot, Plasmodiophora brassicae, Hormone, Cytokinin
INTRODUCTION

Clubroot disease, caused by Plasmodiophora brassicae Woronin, is a serious concern for growers of Brassicaceae crops and is one of the most common diseases of oilseed rape in North America and Europe (Robak 1991; Agrios 2005; Dixon 2009; Lüders et al. 2011). The pathogen P. brassicae belonging to plasmodiophorids of the eukaryote supergroup Rhizaria, is an obligate biotrophic protist which is distinctively different from other plant pathogens such as fungi or oomycetes. There exists wide diversity in the population of this pathogen which enables it to overcome the resistance shown by different crop species including Brassica oleracea or Brassica rapa (Jones et al. 1982; Some et al. 1996). The pathogen has substantial variability in Korea as well (Kim et al. 2016). Kim et al. (2016) recently grouped 12 Korean field isolates of P. brassicae into four pathotypes based on their reactions to the Williams’ differential set: pathotypes 1 (Gangneung 1, Gangneung 2, Goesan, Jeongseong and Hoengseong), 2 (Daejon and Keumsan), 3 (Haenam 1, Pyeongchang, Yeoncheon) and 4 (Haenam 2 and Seosan). A Japanese clubroot-resistant (CR) cultivar Akimeki exhibits resistance to all but two (Haenam 2 and Seosan) Korean field isolates. Ribosomal DNA sequencing revealed that these isolates have variable nucleotide sequences in the smaller subunit of intron 1 (Laila et al. 2017). Due to this pathotype diversity, the disease severity of clubroot disease vary greatly among different regions. A severe outbreak of clubroot disease in Korean Chinese cabbage, the most important ingredient of the famous Korean dish, baechu kimchi, was reported in the last decade (Cho and Kenji 2003). The outbreak of clubroot disease is predominantly being recorded to be resulted from movement of infested soil, plant materials and other farm machineries (Strelkov and Hwang 2014).

P. brassicae is obligatory in nature and has a complex life cycle having two distinct zoosporic stages namely, formation of plasmodia and formation of resting spore inside host cells (Fig. 1). The infection process of P. brassicae can generally be separated into two distinct phases, primary infection and secondary infection, based on the nature of the infection and the type of root being infected. The primary infection stage is generally the first 72 hours of pathogen attack when the zoospores, released by the haploid resting spore, infect root hairs (Fig. 1) (Dekhuijzen 1981; Müller and Hilgenberg 1986). Subsequently, the secondary phase of infection occurs when the zoospores invade the root cortex and steles of both the hypocotyls and roots of infected plants and develop secondary multinucleate plasmodia. Plasmodia causes rapid cell proliferation (hyperplasia) and abnormal cell enlargement (hypertrophy) which eventually results in the development of abnormal growth of root tissues, commonly known as ‘galls’. At severe cases, galls disrupt the usual water and nutrient transport in the root leading to permanent wilting of plants. The abundance and durability of spores and lack of suitable chemical control measures makes it difficult to control the disease. The extensive cell division and cell enlargement that occur in galls during secondary infection phase is due to altered hormonal balance, mainly of Auxin and cytokinin in root tissues (Dekhuijzen and Overeem 1971; Butcher et al. 1974). Here, we discuss the role of cytokinins and genes responsible for cytokinin biosynthesis on clubroot disease development.

Plasmodiophora brassicae mediates hormone homeostasis in host plants

Studies on interaction of plants with symbiotic or pathogenic microorganisms indicated differential roles of plant’s defense-related hormones in aerial (e.g., leaves) and underground (e.g., roots) organs (Vysotskaya et al. 2008; Tytgat et al. 2013; Sasaki et al. 2014; Jing and Strader 2019). In particular, auxins and cytokinins, besides having differential developmental roles in roots and shoots have also been recently shown to have divergent defense responses in roots; either independently, or depending on other defense-related hormones such as jasmonic acid and salicylic acid (Naseem and Dandekar 2012; Chen et al. 2014; Boivin et al. 2016). Plant pathogens have developed different strategies to establish successful infection by foiling plants defense responses, which includes mediating phytohormonal responses to their advantage (Robert-Seilaniantz et al. 2011; Pieterse et al. 2012; De Vleesschauwer et al. 2014). Some pathogens such as P. brassicae and Agrobacterium tumefaciens can produce phytohormones themselves (Müller and Hilgenberg 1986) that can alter growth and development of host plants in a way to facilitate invasion and colonization of pathogens, and to hijack host nutrients by forming new source-sink relationship (Boivin et al. 2016).

Plant tissue infected with P. brassicae has been shown to modify the balance of at least four plant hormones namely, cytokinins, auxins, salicylic acid and jasmonic acid (Schwelm et al. 2015). Phytohormone homeostasis in hypertrophied roots due to P. brassicae invasion at the beginning of gall formation have been a focus of investigation over the past years. The pathogen-driven interference of the plant root phytohormone system, particularly the alterations in the two major hormone groups, auxins (Butcher et al. 1974) and cytokinins (Dekhuijzen 1981), are found to induce hypertrophy and cell divisions by reprogramming existing meristematic activity in infected host roots leading to formation of gall (Fig. 1) (Ludwig-Müller 1999; Siemens 2006; Malinowski et al. 2012; Boivin et al. 2016).

Cytokinin as key hormone in clubroot resistance

Cytokinins are key plant hormones, known to play major roles in various biological processes including growth, development, plant morphogenesis, metabolism and nutrient assimilation and translocation etc. (Gan and Amasino 1995; Mok and Mok 2001; Sakakibara 2006). Chemically, natural cytokinins are N6-substituted purine derivatives. In plants, cytokinins are predominantly found as kinetin, zeatin and 6-benzylaminopurine (Hwang et al. 2012). Cytokinins are also known to play pivotal roles in integrating diverse environmental stress responses and in plant’s immunity against pathogenic microbes (reviewed Choi et al. 2011; Denancé et al. 2013; Giron et al. 2013; Naseem et al. 2014) and insect pests (Jameson 2000; Mapes and Davies 2001; Stone and Schönrogge 2003; Sakakibara 2006; Giron et al. 2007; Schwachtje and Baldwin 2008; Dervinis et al. 2010).

Against clubroot, roles of key plant hormones, especially cytokinins and auxins have been extensively investigated in the past decades (reviewed in Giron et al. 2013; Boivin et al. 2016; Malinowski et al. 2016). Club growth or gall formation has been speculated to be the overall result of auxin and cytokinin homeostasis (Ludwig-Müller et al. 2009; Schuller et al. 2014; Jia et al. 2017; Ludwig-Müller et al. 2017; Ciaghi et al. 2018). Elevated levels of cytokinins and increased cell division were observed in the early stages of P. brassicae infection in Arabidopsis thaliana. But at the later stages of gall formation, decreased levels of cytokinins and repressed expressions of host cytokinin biosynthetic genes mainly cytokinin oxidases and dehydrogenases were observed (Devos et al. 2006; Siemens et al. 2006; Malinowski et al. 2016). Cytokinin responsiveness was induced during the initial stages (3 days after inoculation, dai) of clubroot disease in the cortex and vascular tissues of the infected root and hypocotyls (visualized by ARR5:GUS expression), which was then observed in all cell layers from 5 dai onwards throughout the period of gall formation (Devos and Prinsen 2006; Siemens et al. 2006). Overexpression of AtCKX harboring cytokinin-inducible promoter ARR5 gene in A. thaliana caused downregulation of cytokinins, whereas downregulation of AtCKX and AtADK were associated with higher levels of active cytokinins during P. brassicae infection (Siemens et al. 2006; Ludwig-Müller et al. 2009). These further confirms the role of cytokinins in plants resistance to P. brassicae.

In turnip (B. rapa) as well, cytokinin levels were higher in infected roots compared to healthy roots (Dekhuijzen 1981). Plasmodia of P. brassicae are also believed to produce minute amounts of cytokinins, which are released into the cytoplasm of the host cells during invasion that helps in the proliferation of root tissues (Fig. 1) (Dekhuijzen 1981; Müller and Hilgenberg 1986). This is further supported by the finding that isopentenyl transferase genes (BrIPT1, 3, 5 and 7) are transiently expressed at high levels in host tissues prior to gall formation which during during gall formation were found to be downregulated, suggesting that pathogen-induced cytokinin production triggers gall formation (Ando et al. 2005). Besides, cytokinins were also found to interfere with the production of invertase and sugar metabolism which might be crucial for the nutrition of P. brassicae (Siemens et al. 2011). However, laser microdissection and pressure catapulting (LMPC) analysis revealed the upregulation of genes involved in auxin and cytokinin metabolism during this process (Schuller et al. 2014). The fluctuation in plant hormone contents does not correspond to the severity of infection in cabbage roots (Schuller and Ludwig-Müller 2006). Transcriptome analysis during the root hair infection phase preceding infection of the cortex revealed only a small number of genes with altered expression in A. thaliana (Agarwal et al. 2011). By contrast, comparisons of the transcriptomes of the root cortex during two time points of the secondary infection phase revealed numerous up- and downregulated genes (Siemens et al. 2006). Some root-specific cytokinin oxidase genes were down-regulated in root gall tissues compared with the controls (Siemens et al. 2006), whereas some were upregulated at a later time point of infection (Schuller et al. 2014). Understanding the detailed roles of the key cytokinin related genes mainly, cytokinin oxidase/dehydrogenases (CKXs) and isopentenyl transferases (IPTs) during clubroot infection and gall expansion in plants, especially in commercially important crops like canola and cabbage will be crucial for improving crops resistance towards the disease.

Properties and functions of Cytokinin oxidase/dehydrogenases

Cytokinin oxidase/dehydrogenases (CKXs) is responsible in catalyzing irreversible degradation of cytokinin (Brownlee et al. 1975; Armstrong 1994; Kakimoto 2001). In this process of degradation of cytokinin and their derivatives, these enzymes remove N6-substituted isoprene chains of isopentenyladenine and isopentenyladenine riboside (Galuszka et al. 2000; Motyka et al. 2003). In the catalytic process, the CKX enzymes which act as electron acceptors, display a dual catalytic mode in association with molecular oxygen and other specific substances (Frebortova et al. 2004). These enzymes show greater thermo-stability whereas optimum pH requirement was found to be substrate dependent (Kopecný et al. 2005). As CKXs enzyme bear both flavin adenine dinucleotide (FAD) and CK-binding domains, these enzymes might act as a substitute of flavin enzymes (Esparza and Morris 2001). Moreover, post-translational glycosylation of CKX proteins might alter their molecular masses and localization (Motyka et al. 2003).

CKX is a small gene family that encodes CKX proteins (Werner et al. 2006). CKX family genes and putative members were found to be functionally expressed in the members of both Brassicaceae family such as B. rapa (Liu et al. 2013), A. thaliana (Galuszka et al. 2007) and several other families. The pivotal roles of the catabolic enzyme cytokinin oxidase (CKX) in controlling the accumulation of cytokinins has been found in various tissues of many higher plants (Mok 1994).There are seven CKX genes in A. thaliana: AtCKX1–AtCKX7 those differ not only in their subcellular localizations and biochemical characteristics but also in their expression patterns. Experimental evidences suggest that diverse functions of CKXs might be associated with spatial and temporal expression patterns, since in transgenic Arabidopsis reduced cytokinin levels and developmental changes in roots and shoots are reported (Werner et al. 2003; Galuszka et al. 2007). In B. napus, hormonal treatments altered responses of CKX genes (Liu et al. 2018). Our unpublished data showed that five CKX genes showed variation in expression both in roots and shoots. Moreover, expression level of genes differed greatly before and after gall development in B. rapa indicating that CKX genes have vital role in clubroot disease development.

Properties and functions of Isopentenyl transferases (IPTs)

In A. thaliana, two classes of Isopentenyl transferases (IPTs) are evident based on the use of substrates: AtIPT1, 3, 4–8 encode forms that use ADP/ATP as substrates whilst AtIPT2 and 9 encode forms that use tRNA as substrates (Miyawaki et al. 2006). IPTs are involved in rate limiting steps in cytokinin biosynthesis (El-Showk et al. 2013). The IPTs synthesized from ADP/ATP are the active enzymes whilst IPTs synthesized from tRNA shows limited activity in A. thaliana (Gajdošová et al. 2011). Similar to CKXs, the IPTs also show spatial and temporal variation in level of expression. In P. brassicae infected plants two genes; IPT3 and IPT5 exhibited abundant expression in both root and hypocotyl tissue but the expression level was greatly (8 folds) reduced in infected tissues compared to un-infected tissues (Malinowski et al. 2016). This results speculatively indicated that the repressed expression of these two genes might be associated with transcriptional regulation rather than alterations in the proportion of specific cell types. Compared to IPT3 and IPT5, the expression of IPT1 and IPT7 was reduced and thus, it is evident that these two genes, IPT1 and IPT7, might have insignificant contribution in cytokinin biosynthesis. Similarly, a lower expression of IPT2 and IPT9 genes both in infected and un-infected tissues also indicated that those two genes also have less contribution in gall formation (Malinowski et al. 2016).

Contribution of P. brassicae on cytokinin content

P. brassicae has two IPT genes whose substrate specificity are yet to be characterized. However, these two genes show greater sequence homology to tRNA IPTs. Both of these two genes were expressed at both 16 and 26 days post-inoculation (dpi) suggesting that these two genes contributes in cytokinin accumulation in infected tissue (Malinowski et al. 2016). In ipt1;3;5;7 mutants, cytokinin biosynthesis was greatly compromised due to reduced expression of ARR4–7 genes and as a result, secondary infection of clubroot was reduced. Microarray analysis confirmed that reduction of infection was not due to a compensatory increase in expression of other host IPT genes, since ipt1;3;5;7 genes showed no change in expression. Isolated plasmodia are able to take up radio labelled adenine and able to make small amounts of a compound that are designated as tZ (Müller and Hilgenberg 1986). However, the amount of tZ being released, stimulating type A ARR genes expression in the ipt1;3;5;7 mutant, is not sufficient to rescue mutant phenotype from restoring vascular cambium development. Thus, it can be postulated that the amount of cytokinin produced by P. brassicae have minor contribution on the development of its host. In ipt1;3;5;7 mutant disease development was restricted through restricting hyperplasia but infected cells still show hypertrophy symptom. Gibberellic acid (GA) has no effect on gall formation (Päsold and Ludwig-Müller 2013) but brassinosteroid (BR) biosynthesis influence gall formation (Schuller et al. 2014). Cytokinins have an important role in the development of P. brassicae. Vascular cambial activity is required for gall to be formed and the infection by the pathogen is not dependent on this activity (Malinowski et al. 2012).

Enhancing plant’s resistance: prospects of cytokinin related transgenes

Improving plants resistance to diseases via transgenic (Chen et al. 2012; Jones et al. 2014; Saharan et al. 2016) and recent genome editing based technologies (Andolfo et al. 2016; Borrelli et al. 2018; Langner et al. 2018; Yin and Qiu 2019) are well established. In this regard, the cytokinin related genes may be crucial in improving clubroot resistance in Brassica crops as the accumulation of hormones mainly, cytokinins, auxins and brassinosteroids, especially in secondary infection phase, are associated with progress of the disease (Siemens et al. 2006; Jahn et al. 2013; Schuller et al. 2014). Manipulating those genes will lead to altered accumulation of target hormones which may be helpful in achieving resistance of various degrees to the disease. So far, the contribution of individual hormones in the development of clubroot has been studied by using few key auxin and cytokinin related transgenic lines, summarized in Table 1 (Grsic-Rausch et al. 2000; Siemens et al. 2006; Jahn et al. 2013). Overexpression of a cytokinin degrading proteins (encoded by cytokinin oxidase/dehydrogenase) in transgenic or mutant A. thaliana lines have shown elevated resistance to clubroot against four isolates of P. brassicae (Schuller et al. 2014). In addition, auxin and cytokinin responsive promoter::reporter lines were shown to activate auxin and cytokinin response (Devos et al. 2006; Päsold et al. 2010; Schuller et al. 2014).

Overexpression of isopentenyl transferase genes in PSAG12 ::IPT and PSAG13 ::IPT lines of A. thaliana showed elevated resistance to necrotrophic fungus Botrytis cinerea, causing botrytis bunch rot or grey mould in horticultural crops (Swartzberg et al. 2008). Overexpression of cytokinin-activated transcription factor ARR2 have shown to enhance cytokinin levels, delay leaf senescence and increase resistance to Pseudomonas syringae (Choi et al. 2010). In Brassicaceae crops, transgenic studies using key cytokinin related genes remains to be done. However, transgenic B. rapa line (Crr1aG004 promoter::Crr1aG004) overexpressing TIR-NB-LRR–type R genes Crr1a induced resistance to clubroot in a susceptible cultivar (Hatakeyama et al. 2013). The variable role of cytokinins and associated genes in different pathosystems calls for further research to identify resistant cytokinin gene mediated plant and pathogen interaction (Hirani et al. 2015; Nafisi et al. 2015; Ludwig-Müller et al. 2017; Ciaghi et al. 2018).

Conclusion and perspective

Cytokinin is required for P. brassicae for its development. Pathogen itself produce minute amount of cytokinin and withdraw cytokinin from its host. Vascular cambial (VC) development of the host tissue, dependent on cytokinin, is essential for secondary development and active growth of plants. However, utilization of host’s cytokinin and obstruction of VC route via forming galls by P. brassicae disrupts plants normal growth and development. Wider understanding of the mechanism of disease development and plants defense strategy require further investigation on complex homeostasis of cytokinins with other hormones such as auxins and brassinosteroids. The exact roles of the genes related with cytokinin synthesis or degradation against various pathotypes along the process of disease development remains to be determined. The genes that lie within the already identified QTLs in various crop plants especially in Brassica species may hold the key for improving resistance to clubroot disease in crop plants.

ACKNOWLEDGEMENTS

This paper was supported by Sunchon National University Research Fund in 2019.

Figures
Fig. 1. The life cycle of Plasmodiophora brassicae and the possible integration of cytokinin signaling pathways by this pathogen during clubroot formation (after Dekhuijzen 1981; Müller and Hilgenberg 1986 1986). dpi = days post inoculation.
Tables

Transgenic Arabidopsis lines showing elevated resistance against Plasmodiophora brassicae and other phytopathogens upon overexpression of cytokinin related genes.

Genez) Line/Mutant Pathogen (isolate) Reference
Cytokinin oxidase/dehydrogenases 35S::AtCKX1 P. brassicae (1CK) Siemens et al. 2006
P. brassicae (e2)
P. brassicae (eH)
P. brassicae (k1)
35S::AtCKX3 P. brassicae (1CK)
P. brassicae (e2)
P. brassicae (eH)
P. brassicae (k1)
Isopentenyl transferase PSAG12 ::IPT B. cinerea Swartzberg et al. 2008
PSAG13 ::IPT B. cinerea
Cytokinin-activated transcription factor 35S:ARR2 P. syringae Choi et al. 2010
Differential disease response of different transgenic lines overexpressing other genes are comprehensively presented in Alix et al. (2007), Diederichsen et al. (2009), and Ludwig-Müller et al. (2017).

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