Cytokinins as key regulators in plant–microbe–insect interactions: connecting plant growth and defence

Abstract

Summary1. Plant hormones play important roles in regulating plant growth and defence by mediating developmental processes and signalling networks involved in plant responses to a wide range of parasitic and mutualistic biotic interactions. 2. Plants are known to rapidly respond to pathogen and herbivore attack by reconfiguring their metabolism to reduce pathogen/herbivore food acquisition. This involves the production of defensive plant secondary compounds, but also an alteration of the plant primary metabolism to fuel the energetic requirements of the direct defence. 3. Cytokinins are plant hormones that play a key role in plant morphology, plant defence, leaf senescence and source-sink relationships. They are involved in numerous plant-biotic interactions. 4. These phytohormones may have been the target of arthropods and pathogens over the course of the evolutionary arms race between plants and their biotic partners to hijack the plant metabolism, control its physiology and/or morphology and successfully invade the plant. In the case of arthropods, cytokinin-induced phenotypes can be mediated by their bacterial symbionts, giving rise to intricate plant-microbe-insect interactions. 5. Cytokinin-mediated effects strongly impact not only plant growth and defence but also the whole community of insect and pathogen species sharing the same plant by facilitating or preventing plant invasion. This suggests that cytokinins (CKs) are key regulators of the plant growth-defence trade-off and highlights the complexity of the finely balanced responses that plants use while facing both invaders and mutualists.

Leaf-Miners Co-opt Microorganisms to Enhance their Nutritional Environment

“…However, the sugar profiles in mined tissues on green and yellow leaves are similar despite different amount of CKs. This confirms that not only are CK quantities in various plant tissues important but, also important are (i) the type of CKs, which may differ if they are originating from the plant or from the biotic invaders; (ii) the nature of the target cells/tissues; (iii) the developmental state of the plant; and (iv) the hormonal balance between CKs and other phytohormones such as auxin (Farnsworth 2004;Frebort et al 2011;Giron et al 2013;Hare et al 1997). How the CK signal evolves over the course of the insect development (regarding successive larval stages with different requirements and/or feeding habit for example) and how this impacts the plant primary and secondary metabolism also remains to be investigated (Giron et al 2013).…”

“…The second hypothesis is supported by the absence of altered CKs profiles in the mine when larvae are cured from their endosymbionts (and then do not contain CKs themselves). The ability to produce CKs has been demonstrated clearly in different plant-associated organisms including bacteria, fungi, nematodes, and herbivorous insects (Frugier et al 2008;Giron et al 2013;Walters et al 2008). A conclusive demonstration of the exact origin of CKs in our system would require complex genome-wide sequencing and/or labelling approaches.…”

“…They are key regulators in plant-insect-microbe interactions and play a central role in plant colonization and exploitation by various plant-associated organisms, including both antagonists and mutualists (Giron et al 2013). These phytohormones may have been the targets of arthropods and pathogens over the course of the "evolutionary arms race" between plants and their biotic partners to "hijack" plant metabolism and development enabling them to successfully invade the plant.…”

“…There has been considerable debate about the likely origin of CKs in infected leaves, as it is not yet clear whether they are produced by the pathogen/insect or by the plant. Indeed, pathogens and herbivorous insects potentially influence the levels of phytohormones by inducing plant genes involved in CK biosynthesis, degradation, or response, but they also can produce and secrete relevant phytohormones themselves (Farnsworth 2004;Giron et al 2013;Jameson 2000;Robert-Seilaniantz et al 2007;Walters et al 2008). In the case of arthropods, CK-induced phenotypes can be mediated by their bacterial symbionts, giving rise to intricate plantmicrobe-insect interactions (Kaiser et al 2010).…”

“…In these islands, nutrientsmainly sugars -are redirected towards the infection site where host cell death is delayed. As CKs strongly impact plant sugar metabolism, biotic invaders can specifically affect CKs, thus redirecting plant resources for their own benefit (Giron et al 2013;Lara et al 2004). Indeed, these phytohormones have been found to induce expression of extracellular invertases and hexose transporters that result in the transport and accumulation of nutrients at infection sites (Ehneß and Roitsch 1997;Godt and Roitsch 1997;Mothes 1964;Lara et al 2004).…”