Cytokinin : a developing story

In the past decade tremendous advances have been made in understanding the biosynthesis, perception, and signaling pathways of the plant hormone cytokinin. It also became clear that interfering with any of these steps greatly impacts all on stages of growth and development. This has recently spurted renewed effort to understand how cytokinin signaling affects developmental processes. As a result, new insights on the role of cytokinin signaling and the downstream targets during, for example, shoot apical meristem, flower, female gametophyte, stomata and vascular development are being unraveled. In this review we aim to give a comprehensive overview of recent findings on how cytokinin influences growth and development in plants, and highlight areas for future research

Vascular transcription factors guide plant epidermal responses to limiting phosphate conditions

Optimal plant growth is hampered by deficiency of the essential macronutrient phosphate in most soils. Plant roots can, however, increase their root hair density to efficiently forage the soil for this immobile nutrient. By generating and exploiting a high-resolution single-cell gene expression atlas of Arabidopsis roots, we show an enrichment of TARGET OF MONOPTEROS 5 / LONESOME HIGHWAY (TMO5/LHW) target gene responses in root hair cells. The TMO5/LHW heterodimer triggers biosynthesis of mobile cytokinin in vascular cells and increases root hair density during low phosphate conditions by modifying both the length and cell fate of epidermal cells. Moreover, root hair responses in phosphate deprived conditions are TMO5 and cytokinin dependent. In conclusion, cytokinin signaling links root hair responses in the epidermis to perception of phosphate depletion in vascular cells

Diffusible repression of cytokinin signalling produces endodermal symmetry and passage cells.

In vascular plants, the root endodermis surrounds the central vasculature as a protective sheath that is analogous to the polarized epithelium in animals, and contains ring-shaped Casparian strips that restrict diffusion. After an initial lag phase, individual endodermal cells suberize in an apparently random fashion to produce 'patchy' suberization that eventually generates a zone of continuous suberin deposition. Casparian strips and suberin lamellae affect paracellular and transcellular transport, respectively. Most angiosperms maintain some isolated cells in an unsuberized state as so-called 'passage cells', which have previously been suggested to enable uptake across an otherwise-impermeable endodermal barrier. Here we demonstrate that these passage cells are late emanations of a meristematic patterning process that reads out the underlying non-radial symmetry of the vasculature. This process is mediated by the non-cell-autonomous repression of cytokinin signalling in the root meristem, and leads to distinct phloem- and xylem-pole-associated endodermal cells. The latter cells can resist abscisic acid-dependent suberization to produce passage cells. Our data further demonstrate that, during meristematic patterning, xylem-pole-associated endodermal cells can dynamically alter passage-cell numbers in response to nutrient status, and that passage cells express transporters and locally affect the expression of transporters in adjacent cortical cells

Arabidopsis RCD1 coordinates chloroplast and mitochondrial functions through interaction with ANAC transcription factors

Reactive oxygen species (ROS)-dependent signaling pathways from chloroplasts and mitochondria merge at the nuclear protein RADICAL INDUCED CELL DEATH 1 (RCD1). RCD1 interacts in vivo and suppresses the activity of the transcription factors ANAC013 and ANAC017, which mediate a ROS-related retrograde signal originating from mitochondrial complex III. Inactivation of RCD1 leads to increased expression of mitochondrial dysfunction stimulon (MDS) genes regulated by ANAC013 and ANAC017. Accumulating MDS gene products, including alternative oxidases (AOXs), affect redox status of the chloroplasts, leading to changes in chloroplast ROS processing and increased protection of photosynthetic apparatus. ROS alter the abundance, thiol redox state and oligomerization of the RCD1 protein in vivo, providing feedback control on its function. RCD1-dependent regulation is linked to chloroplast signaling by 3'-phosphoadenosine 5'-phosphate (PAP). Thus, RCD1 integrates organellar signaling from chloroplasts and mitochondria to establish transcriptional control over the metabolic processes in both organelles

The transcription factor AtMYB12 is part of a feedback loop regulating cell division orientation in the root meristem vasculature

Transcriptional networks are crucial to integrate various internal and external signals into optimal responses during plant growth and development. Primary root vasculature patterning and proliferation are controlled by a network centred around the basic Helix-Loop-Helix transcription factor complex formed by TARGET OF MONOPTEROS 5 (TMO5) and LONESOME HIGHWAY (LHW), which control cell proliferation and division orientation by modulating cytokinin response and other downstream factors. Despite recent progress, many aspects of the TMO5/LHW pathway are not fully understood. In particular, the upstream regulators of TMO5/LHW activity remain unknown. Here, using a forward genetic approach to identify new factors of the TMO5/LHW pathway, we discovered a novel function of the MYB-type transcription factor MYB12. MYB12 physically interacts with TMO5 and dampens the TMO5/LHW-mediated induction of direct target gene expression as well as the periclinal/radial cell divisions. The expression of MYB12 is activated by the cytokinin response, downstream of TMO5/LHW, resulting in a novel MYB12-mediated negative feedback loop that restricts TMO5/LHW activity to ensure optimal cell proliferation rates during root vascular development

Gibberellins promote polar auxin transport to regulate stem cell fate decisions in cambium

Vascular cambium contains bifacial stem cells, which produce secondary xylem to one side and secondary phloem to the other. However, how these fate decisions are regulated is unknown. Here we show that the positioning of an auxin signalling maximum within the cambium determines the fate of stem cell daughters. The position is modulated by gibberellin-regulated, PIN1-dependent polar auxin transport. Gibberellin treatment broadens auxin maximum from the xylem side of the cambium towards the phloem. As a result, xylem-side stem cell daughter preferentially differentiates into xylem, while phloem-side daughter retains stem cell identity. Occasionally, this broadening leads to direct specification of both daughters as xylem, and consequently, adjacent phloem-identity cell reverts to being stem cell. Conversely, reduced gibberellin levels favour specification of phloem-side stem cell daughter as phloem. Together, our data provide a mechanism by which gibberellin regulates the ratio of xylem and phloem production.Auxin is a key regulator in vascular cambium development. This study shows that gibberellins promote polar auxin transport along the root, which leads to broadening of high auxin signalling domain in cambium, and thus, to increased xylem formation.Peer reviewe

DOF2.1 Controls Cytokinin-Dependent Vascular Cell Proliferation Downstream of TMO5/LHW

Smet et al. capture the transcriptional responses upon simultaneous TMO5/LHW induction and identify DOF2.1 as part of the cytokinin-dependent downstream responses. Furthermore, they show that DOF2.1 and its closest homologs control periclinal and radial procambium divisions in distinct zones of this tissue.</p

DOF2.1 controls vascular cell proliferation downstream of TMO5/LHW

As plant cells are fixed within their tissue context, a precise control of cell division orientation is crucial to generate complex three-dimensional organs. The transcription factor complex formed by TARGET OF MONOPTEROS5 (TMO5) and LONESOME HIGHWAY (LHW) triggers a change in cell division orientation leading to radial expansion, at least in part by activating local cytokinin biosynthesis. However, it remains unclear how cytokinin controls these oriented cell divisions. Here, we analyzed the transcriptional responses upon simultaneous induction of both TMO5 and LHW in detail. Using inferred network analysis, we identify AT2G28510/DOF2.1 as a cytokinin-dependent downstream target gene of the TMO5/LHW heterodimer complex. We further show that DOF2.1 is specifically required and sufficient for vascular cell proliferation without inducing other cytokinin-dependent effects such as the inhibition of vascular differentiation. In summary, we have identified DOF2.1 as a TMO5/LHW target gene, specifically responsible for controlling vascular cell proliferation leading to radial expansion. Overall design: 4-day-old pRPS5A::TMO5:GR x pRPS5A::LHW:GR (dGR) plants grown on MS were treated with dexamethasone (DEX) compounds for the indicated time, whereafter root meristems were harvested, and total RNA was isolated that was subjected to gene expression profiling