Plants have the ability to recognize beneficial and pathogenic microorganisms. They can promote or limit their colonization as it is crucial for their survival. Plant hormones regulate plant microbe interactions, coordinate cellular and metabolic responses in relation to colonization by microorganisms (Boivin et al., 2016). Activation of plant immunity require signaling and control. As soon as the plant detects pathogen attack, the information is communicated through molecular signaling network to activate immune response. The signaling network is highly interconnected and the common network component mediate different signaling event to inhibit each other (Sato et al., 2010). The signaling network are modulated in order to help plant to mitigate infection. The synergism between CK and SA promote defense against biotrophs. CK may promote jasmonic acid (JA); however in a feedback loop JA suppresses CK responses. The cross talk between auxin and cytokinin may have an antagonistic effect on plant immunity (Naseem et al., 2015). Insect or pathogen attack is followed by enhanced level of cytokinins (CKs) at the infection site. Increased accumulation of CK at infection site may decrease energy supply for plant growth but can fuel the plant defense machinery, suggesting that that these molecule play a key role in reconfiguration of the primary and secondary metabolism associated with plant –induced defense (Giron et al., 2013).
Cytokinin phytohormone stimulate cell division and are involved in embryonic cells, maintenance of meristematic cells, shoot formation and development of vasculature. This (CK) phytohormone is not only essential for plant growth and development but also impacts plant immunity (Wang et al., 2017). CK works as a major factor in plant-microbe interaction during nodule organogenesis and pathogenesis. Plant-borne cytokinins systemically induce resistance against pathogen infection. This resistance is by endogenous CK and salicylic acid (SA) signaling (Choi et al., 2011). Plant pathogens manipulate the endogenous CK and/or auxin content of their host plant (Jameson 2000).
The CK signaling pathway regulates reactive oxygen species (ROS) and homeostasis in guard cells which leads to enhanced stomatal immunity and plant resistance to bacteria (Arnaud et al., 2017). Stomata play a critical role in plant immunity. Upon pathogen attack or pathogen-associated molecular patterns (PAMPs) plants close their stomata to prevent invasion of pathogen and colonize the host tissue (Melotto et al., 2006). In turn pathogen virulence factor such as the phytotoxin coronatine (COR) secreted by the bacterial pathogen Pseudomonas syringae pv tomato (Pst) strain DC3000 suppresses host stomatal defenses and further advance stomatal reopening (Melotto et al., 2006).
Plant hormone change host immunity. The concentration of CK regulates defense responses in a positive or a negative manner i.e. cytokinin level influence the outcome of plant-pathogen interactions. Argueso et al. (2012) observed that high concentration of CK lead to increased defense responses to a virulent oomycete pathogen, through SA accumulation and activation of defense gene expression. Lower concentration of CK results in increased pathogen growth. Novak et al. (2013) suggested that plant can produce sufficiently high levels of cytokinins to trigger fast cell death without any interveining chlorosis- symptom for hypersensitive response. The chloroplastic hydrogen peroxide stimulates hypersensitive-like response, including inhibition of photosynthesis, elevated levels of stress hormones, oxidative membrane damage and stomatal closure.
The cross talk between CK and SA signaling network regulate plant defense responses against pathogens. Plant pathogen can trigger symptoms that indicate hormonal disorders, formation of galls, cankers of trees and premature senescence (so called green islands) in plants (Grant and Jones 2009). Pathogen can secrete CKs themselves or induce CK biosynthesis in plants or both leading to the suppression of plant immunity (Spallek et al., 2018). The accumulation of CK induces production and accumulation of phytoalexins in a SA-independent manner enhancing SA-dependent immunity (O’Brien and Benkova 2013). High CK levels, induced after the pathogen attack, activate CK signaling pathway which regulates pathogenesis related protein 1 (PR1), PR3, PR4 and PR5 expression hence promotes plant immunity (Naseem et al., 2012; O’Brien and Benkova 2013).
Cytokinins and auxins are known to act antagonistically, but a synergistic interaction between auxin and cytokinin also exists (Schaller et al., 2015). Jiang et al. (2013) reported CK accumulation after infection by blast fungus Magnaporthe oryzae . Fungus elevates rice CK levels for its own benefit such as mobilizing nutrients towards the infection site. On the other hand rice plant, sense CK accumulation as an infection signal and induces defense responses by acting synergistically with SA. Auxin inhibits CKs ranging from its biosynthesis to the suppression of its signaling (Naseem and Dandekar 2012). Cytokinin induced resistance is mediated by increased antimicrobial phytoalexin production (Grosskinsky et al., 2011). This demonstrates that auxin, abscisic acid, gibberellins and cytokinin cross communicate with the central ethylene-salicylic acid-jasmonic acid signal transduction pathway in immunity. The two phytoalexin such as scopoletin and capsidiol are often restricted to infected tissue (Grosskinsky et al., 2011). Interestingly despite the absence of hypersensitive response, the increased level of CK induce bactericidal activities controlling bacterial growth. Plant needs to balance the two conflicting demands: efficiently abolish the pathogen infection and limit the negative impacts of immune responses on plant health (tissue integrity, photosynthetic capacity and primary metabolism) (Sato et al., 2010). High level of defense activation leads to reduced growth and reduced seed set. Impact of cytokinin has been observed on various aspects of plant immunity.
See Part IV for further information
Argueso, C. T., Ferreira, F. J., Epple, P., To, J. P., Hutchison, C. E., Schaller, G. E., Dangl, J. L. and Kieber, J. J. 2012 Two-component Elements Mediate Interactions between Cytokinin and Salicylic Acid in Plant Immunity. PLoS 8(1):e1002448
Arnaud, D., Lee, S., Takebayashi, Y., Choi, D., Choi, J., Sakakibara, H. and Hwang, I. 2017 Cytokinin-Mediated Regulation of Reactive Oxygen Species Homeostasis Modulates Stomatal Immunity in Arabidopsis. The Plant Cell 29(3): 543 – 559
Boivin, S., Fonouni-Farde, C. and Frugier, F. 2016 How Auxin and Cytokinin Phytohormones Modulate Root Microbe Interactions. Front Plant Sci. 7: 1240
Choi, J., Choi, D., Lee, S., Ryu, C-M R and Hwang, I. 2011 Cytokinins and Plant Immuinty: Old Foes or New Friends? Trends Plant Sci. 16(7): 388-394
Grant, M. R. and Jones, J. D. G. 2009 Hormone (Dis)harmony Moulds Plant Health and Disease. Science 324: 750 – 752
Giron, D., Frago, E., Glevarec, G., Pieterse, C. M. J. and Dicke, M. 2013 Plant-Microbe Interactions Cytokinins as Key Regulators in Plant-Microbe-Insect interactions: Connecting Plant Growth and Defense. Functional Ecology 27: 599 – 609
Grosskinsky, D. K., Naseem, M., Abdelmohsen, U. R., Plickert, N., Engelke, T., Griebel, T., Zeier, J., Novak, O., Strnad, M., Pfeifhofer, H., van der Graaff, E., Simon, U. and Roitsch, T. 2011 Cytokinins Mediate Resistance against Pseudomonas syringae in Tobacco through Increased Antimicrobial Phytoalexin Synthesis Independent of Salicylic Acid Signaling 1[W][OA] . Plant Physiol. 157(2): 815-830
Jameson, P. 2000 Cytokinins and Auxins in Plant-Pathogen Interactions-An Overview. Plant Growth Regul. 32(2-3): 369 – 380
Jiang, C-J., Shimono, M., Sugano, S., Kojima, M., Liu, X., Inoue, H., Sakakibara, H. and Takatsuji, H. 2013 Cytokinins Act Synergistically with Salicylic Acid to Activate Defense Gene Expression in Rice. MPMI 26(3): 287 – 296
Melotto, M., Underwood, W., Koczan, J., Nomura, K. and He, S. Y. 2006 Plant Stomata Function in Innate Immunity against Bacterial Invasion. Cell 126(5): 969 – 980
Naseem, M. and Dandekar, T. 2012 The Role of Auxin-Cytokinin Antagonism in Plant-Pathogen Interactions. PLoS Pathog. 8(11): e1003026
Naseem, M., Philippi, N., Hussain, A., Wangorsch, G., Ahmed, N. and Dandekar 2012 Integrated Systems View on Networking by Hormones in Arabidopsis Immunity Reveals Multiple Crosstalk for Cytokinin. The Plant Cell 24: 1793 – 1814
Naseem, M., Kaltdorf, M. and Dandekar, T. 2015 The Nexus between Growth and Defence Signaling: Auxin and Cytokinin Modulate Plant Immune Response Pathways. Jour. Exp. Bot. 66(16): 4885 – 4896
Novak, J., Pavlu, J., Novak, O., Nozkova-Hlavackova, V., Spundova, M., Hlavinka, J., Koukalova, S., Skalak, J., Cerny, M. and Brzobohaty, B. 2013 High Cytokinin Levels Induce a Hypersensitive-like Response in Tobacco. Annals of Botany 112(1): 41 – 55
O’Brien, J. A. and Benkova, E. 2013 Cytokinin Cross-Talking During Biotic and Abiotic Strress Responses. Front. Plant Sci. 4: 451
Sato, M., Tsuda, K., Wang, L., Coller, J., Watanabe, Y., Glazebrook, J. and Katagiri, F. 2010 Network Modelling Reveals Prevalent Negative Regulatory Relationships between Signaling Sector in Arabidopsis Immune Signaling. PLoS Pathog. 6(7):e1001011
Schaller, G. E., Bishopp, A. and Kieber, J. J. 2015 The Yin-Yang of Hormones: Cytokinin and Auxin Interactions in Plant Development. Plant Cell 27(1): 44 – 63
Spallek, T., Gan, P., Kadota, Y. and Shirasu, K. 2018 Same Tune, Different Song-Cytokinins as Virulence Factors in Plant-Pathogen Interactions? Curr. Opinion Plant Biol. 44: 82 -87
Wang, S., Wang, S., Sun, Q, Yang, L., Zhu, Y., Yuan, Y. and Hua, J. 2017 A Role of Cytokinin Transporter in Arabidopsis Immunity. MPMI 30(4): 325 – 333