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Auxins and cytokinins – the dynamic duo of growth‐regulating phytohormones heading for new shores

2019; Wiley; Volume: 221; Issue: 3 Linguagem: Inglês

10.1111/nph.15556

1469-8137

Dominik K. Großkinsky, Jan Petrášek,

Plant Stress Responses and Tolerance

Pioneers of plant biology such as Charles Darwin and Julius von Sachs had already addressed aspects of phytohormone activities in plant growth and development even before these substances had been discovered, through roles in tropisms (Darwin, 1880; Sachs, 1880). The identification of the first auxin and cytokinin followed some decades later, in the 1920s and 1950s, respectively. Both auxins and cytokinins have been described as essential regulators of diverse plant processes with complex regulations at various levels ranging from biosynthesis to transport and signaling (Sakakibara, 2006; Simon & Petrášek, 2011). In addition, intimate interactions between these two central phytohormones in regulating plant growth and development from the level of the cell to the whole plant have been established (Schaller et al., 2015). Due to the diverse nature of functions and interactions, their activities can best be termed 'complementary' (Schaller et al., 2015). Following this long tradition, a diverse and interacting community of plant scientists is actively working on increasing our understanding of classic functions of these phytohormones, on the identification of integral components regulating their functions, on describing and analyzing novel roles in plant processes unrelated to growth and development, and even functions outside the plant organism (Fig. 1). The International Symposium 'Auxins and cytokinins in plant development … and interactions with other phytohormones' was held in Prague (Czech Republic) in July 2018 under the auspices of the Czech Academy of Sciences (CAS) and the Institute of Experimental Botany CAS. It was the 9th symposium of a series of meetings dealing with phytohormone functions, which was initiated in 1972, and the 5th symposium under this title, which was implemented in 1999. Around 250 participants from 28 countries met to share new results and advancements in the understanding of auxins, cytokinins, their interaction and functions. The symposium comprised plenary and keynote lectures, selected talks and poster presentations on the topics 'Biosynthesis and metabolism', 'Signaling', 'Development', 'Transport', 'Interaction and cross-talk', and 'Interaction with the environment', which stimulated the discussion of future research directions. As central regulators of probably all aspects of plant life, complex signaling pathways of auxins and cytokinins are crucial for their general and specific functions. Therefore, analyzing their signaling components and mechanisms has been a central target of phytohormone research for a long time. Jiří Friml (Institute of Science and Technology, Klosterneuburg, Austria) summarized how our knowledge of auxin-regulated development has advanced during the past two decades and focused on recent work from his laboratory describing the mechanisms of PIN protein polarizations during early embryogenesis, hypocotyl bending and vascular tissue development. The role of transcription factor WRKY23 in the coordination of transcriptional network upstream of PIN polarization (Prát et al., 2018) was shown to be crucial for auxin canalization-driven processes. Moreover, as presented by Matyáš Fendrych (Institute of Science and Technology, Klosterneuburg, Austria), by implementing a sophisticated setup for studying auxin effects on root growth, a nontranscriptional TIR1-dependent signaling branch has been identified. This complements the established TIR1-based transcriptional regulation of auxin responses by a much faster signaling branch, which may explain the rapid response of root growth to auxin mediated by pH changes and calcium signaling (Fendrych et al., 2018). Likewise, signaling and regulatory mechanisms of cytokinins, which mediate the diverse outcomes of their activities in different contexts, need additional exploration as underlined by Joseph Kieber (University of North Carolina, Chapel Hill, NC, USA). In this respect, it is important to consider global impacts of individual signaling components and mechanisms. This is evidenced by the recent finding of genome-wide binding of the type-B Arabidopsis Response Regulator 10 (ARR10), which is induced by cytokinins, and which represents an important mechanism in cytokinin signaling to regulate growth and development (Zubo et al., 2017). The brief 'historical overviews' and novel insights presented by the two plenary speakers, J. Friml and J. Kieber, as well as other speakers show that despite extensive past research, there is much more to learn to achieve a full understanding of cytokinin and auxin signaling. This knowledge is crucial to make these signaling pathways accessible for targeted modulation to improve plant traits. It is well known that phytohormones interact in order to maintain their fine-tuned regulatory functions, which are essential for the roles of auxins and cytokinins in plant growth and development. Therefore, it is important to understand the mechanisms that contribute to 'keeping the balance' of auxin and cytokinin (as well as other phytohormones) homeostasis as highlighted by Karin Ljung (Swedish University of Agricultural Sciences, Umeå, Sweden). It is only by sophisticated mechanisms that the distribution of auxins and cytokinins can be controlled to maintain proper development, as exemplified by distinct auxin and cytokinin gradients in Arabidopsis roots (Petersson et al., 2009; Antoniadi et al., 2015). Besides the homeostasis of cytokinins and auxins, the integration of their signaling is crucial to understand their interaction and function as presented by Ildoo Hwang (University of Science and Technology, Pohang, Republic of South Korea) in the context of vascular cambial activity. During secondary growth, the transcription factor Auxin Response Factor 5 (ARF5) is phosphorylated, mediated by the glycogen synthase kinase 3 BIL1. Subsequently, ARR7 and ARR15 as negative regulators of cytokinin signaling are upregulated (Han et al., 2018). In addition to auxin and cytokinin signaling, this mechanism may also integrate peptide signaling as an important parameter for maintaining cambial activity (Han et al., 2018). These examples underline the relevance of a holistic view on auxins and cytokinins (and other phytohormones), their distribution and signaling. Therefore, simultaneous analysis of these phytohormones is an important approach to address their complex interlinked functions as introduced by Ondřej Novák (Palacký University & Institute of Experimental Botany CAS, Olomouc, Czech Republic). The continuous development of analytical methods led to the establishment of a 'hormonomics platform', which allows for capturing diverse phytohormone levels at the cellular and subcellular level (Šimura et al., 2018). Such approaches will spur on future research into identifying the complex interactions between cytokinins, auxins and other phytohormones. In addition to growth and developmental processes, plants need to regulate responses to and interactions with their environment comprising biotic and abiotic factors, which often cause stress for plants. While other phytohormones have been long established as regulators of stress-related responses, classical growth-regulating phytohormones, such as cytokinins and auxins, are only currently established as modulators of these responses (Großkinsky et al., 2016b). Different crop plants show specific hormonal responses to drought stress as pointed out by Branka Salopek-Sondi (Ruđer Bošković Institute, Zagreb, Croatia). Besides responses of various stress-related hormones such as abscisic acid (ABA), cytokinin and auxin levels also change, which is similar to reported effects of salt stress responses in Brassica rapa (Pavlović et al., 2018). The modulated stress hormones thereby may directly cause alterations in auxin metabolism (Salopek-Sondi et al., 2013). In addition to these novel findings related to abiotic stresses, the function of growth-regulating phytohormones in biotic interactions was addressed during the symposium. While Ibraheem Alimi (Trent University, Peterborough, Canada) explained the relevance of cytokinins in the Ustilago maydis–Zea mays interaction, in which the phytohormones also derive from the fungus (Morrison et al., 2017), Thomas Roitsch (University of Copenhagen, Denmark) introduced different cytokinins as mediators of resistance against the bacterial pathogen Pseudomonas syringae (Großkinsky et al., 2013). Interestingly, this resistance mechanism appears to be integral to the biocontrol ability of a Pseudomonas fluorescens strain, which induces resistance in the host plant by its bacterial cytokinin production (Großkinsky et al., 2016a). Thus, cytokinins can prime plant defense responses as highlighted by Cris Argueso (Colorado State University, Fort Collins, CO, USA), and may integrate resistance mechanisms with growth responses in interaction with other phytohormones such as auxin (Albrecht & Argueso, 2016). The findings of phytohormone production by U. maydis and P. fluorescens as a relevant parameter for their interaction with their host plants was complemented by Megan Aoki (Trent University, Peterborough, Canada) who reported on cytokinin functions in the ameboid slime mould Dictyostelium discoideum. Detailed cytokinin profiling will reveal the function of this phytohormone during the life-cycle of this microbe as it appears to be essential for specific growth stages such as the induction of sporulation (Anjard & Loomis, 2008). The observed phytohormone production, especially including cytokinins and auxins, by a wide range of microbes (Spaepen, 2015) will spur the identification of novel functions of these phytohormones in these organisms and the interaction between them and plants, which is the basis of phytohormones as cross-kingdom communication compounds (Leach et al., 2017). Even though auxins and cytokinins are probably the best-studied phytohormones in plant development, detailed knowledge on central components and mechanisms related to their biosynthesis, regulation and signaling is lacking; this information is needed to fully understand their multifaceted functions. In addition, it becomes evident that their functions are not restricted to plant growth and development, and not even restricted to the plant organism. Therefore, future research needs to further contribute to the elucidation of basic principles integral to the function of these central phytohormonal players in plant growth and development. At the same time, it has to address their functions in stress regulation, interaction and communication with other organisms, and identify potential functions in other organisms as it is indicated by recent findings. These novel research directions could provide information on the role of cytokinins and auxins as messenger molecules between diverse organisms, that is, plants and microbes, which may be important tools in the plant microbiome. In addition, detailed analyzes of the diverse processes regulated by auxins and cytokinins in the plant may allow for the development of phytohormone-based strategies in crop improvement, ultimately combining beneficial traits related to plant growth promotion as well as biotic and abiotic stress resilience. Hence, research on cytokinins and auxins in diverse aspects will, in future contribute to fundamental, translational and applied plant science. The authors would like to thank all participants of the symposium for their excellent contributions, exciting discussions and a fantastic atmosphere during the event, and the Institute of Experimental Botany CAS for its continuing support of the Auxins and Cytokinins in Plant Development (ACPD) symposia. DKG is funded by the Danish Agricultural Agency (grant 34009-15-0964 to B. Veierskov).