Cytokinin action in plant development

Despite long-standing observations on diverse cytokinin actions, the discovery path to cytokinin signaling mechanisms was tortuous. Unyielding to conventional genetic screens, experimental innovations were paramount in unraveling the core cytokinin signaling circuitry, which employs a large repertoire of genes with overlapping and specific functions. The canonical two-component transcription circuitry involves His kinases that perceive cytokinin and initiate signaling, as well as His-to-Asp phosphorelay proteins that transfer phosphoryl groups to response regulators, transcriptional activators, or repressors. Recent advances have revealed the complex physiological functions of cytokinins, including interactions with auxin and other signal transduction pathways. This review begins by outlining the historical path to cytokinin discovery and then elucidates the diverse cytokinin functions and key signaling components. Highlights focus on the integration of cytokinin signaling components into regulatory networks in specific contexts, ranging from molecular, cellular, and developmental regulations in the embryo, root apical meristem, shoot apical meristem, stem and root vasculature, and nodule organogenesis to organismal responses underlying immunity, stress tolerance, and senescence.

/pdf/cytokinin-signaling-networks-3428h56930.pdf

Cytokinin Signaling Networks

The size and activity of the shoot apical meristem is regulated by transcription factors and low molecular mass signals, including the plant hormone cytokinin. The cytokinin status of the meristem depends on different factors, including metabolic degradation of the hormone, which is catalyzed by cytokinin oxidase/dehydrogenase (CKX) enzymes. Here, we show that CKX3 and CKX5 regulate the activity of the reproductive meristems of Arabidopsis thaliana. CKX3 is expressed in the central WUSCHEL (WUS) domain, while CKX5 shows a broader meristematic expression. ckx3 ckx5 double mutants form larger inflorescence and floral meristems. An increased size of the WUS domain and enhanced primordia formation indicate a dual function for cytokinin in defining the stem cell niche and delaying cellular differentiation. Consistent with this, mutation of a negative regulator gene of cytokinin signaling, ARABIDOPSIS HISTIDINE PHOSPHOTRANSFER PROTEIN 6, which is expressed at the meristem flanks, caused a further delay of differentiation. Terminal cellular differentiation was also retarded in ckx3 ckx5 flowers, which formed more cells and became larger, corroborating the role of cytokinin in regulating flower organ size. Furthermore, higher activity of the ckx3 ckx5 placenta tissue established supernumerary ovules leading to an increased seed set per silique. Together, the results underpin the important role of cytokinin in reproductive development. The increased cytokinin content caused an ~55% increase in seed yield, highlighting the relevance of sink strength as a yield factor.

Cytokinin Regulates the Activity of Reproductive Meristems, Flower Organ Size, Ovule Formation, and Thus Seed Yield in Arabidopsis thaliana

The emergence of the tracheophyte-based vascular system of land plants had major impacts on the evolution of terrestrial biology, in general, through its role in facilitating the development of plants with increased stature, photosynthetic output, and ability to colonize a greatly expanded range of environmental habitats. Recently, considerable progress has been made in terms of our understanding of the developmental and physiological programs involved in the formation and function of the plant vascular system. In this review, we first examine the evolutionary events that gave rise to the tracheophytes, followed by analysis of the genetic and hormonal networks that cooperate to orchestrate vascular development in the gymnosperms and angiosperms. The two essential functions performed by the vascular system, namely the delivery of resources (water, essential mineral nutrients, sugars and amino acids) to the various plant organs and provision of mechanical support are next discussed. Here, we focus on critical questions relating to structural and physiological properties controlling the delivery of material through the xylem and phloem. Recent discoveries into the role of the vascular system as an effective long-distance communication system are next assessed in terms of the coordination of developmental, physiological and defense-related processes, at the whole-plant level. A concerted effort has been made to integrate all these new findings into a comprehensive picture of the state-of-the-art in the area of plant vascular biology. Finally, areas important for future research are highlighted in terms of their likely contribution both to basic knowledge and applications to primary industry.

https://www.fs.fed.us/psw/publications/groover/psw_2013_groover004_lucas.pdf

The plant vascular system: evolution, development and functions

https://www.cell.com/trends/plant-science/pdf/S1360-1385(11)00255-X.pdf

Cytokinins: metabolism and function in plant adaptation to environmental stresses

The roots and stems of dicotyledonous plants thicken by the cell proliferation in the cambium Cambial proliferation changes in response to environmental factors; however, the molecular mechanisms that regulate cambial activity are largely unknown The quadruple Arabidopsis thaliana mutant atipt1;3;5;7, in which 4 genes encoding cytokinin biosynthetic isopentenyltransferases are disrupted by T-DNA insertion, was unable to form cambium and showed reduced thickening of the root and stem The atipt3 single mutant, which has moderately decreased levels of cytokinins, exhibited decreased root thickening without any other recognizable morphological changes Addition of exogenously supplied cytokinins to atipt1;3;5;7 reactivated the cambium in a dose-dependent manner When an atipt1;3;5;7 shoot scion was grafted onto WT root stock, both the root and shoot grew normally and trans-zeatin-type (tZ-type) cytokinins in the shoot were restored to WT levels, but isopentenyladenine-type cytokinins in the shoot remained unchanged Conversely, when a WT shoot was grafted onto an atipt1;3;5;7 root, both the root and shoot grew normally and isopentenyladenine-type cytokinins in the root were restored to WT levels, but tZ-type cytokinins were only partially restored Collectively, it can be concluded that cytokinins are important regulators of cambium development and that production of cytokinins in either the root or shoot is sufficient for normal development of both the root and shoot

https://www.pnas.org/content/pnas/105/50/20027.full.pdf

Cytokinins are central regulators of cambial activity

The phytohormone auxin plays a central role in many aspects of plant growth and development. IAA is the most studied natural auxin that possesses the property of polar transport in plants. Phenylacetic acid (PAA) has also been recognized as a natural auxin for >40 years, but its role in plant growth and development remains unclear. In this study, we show that IAA and PAA have overlapping regulatory roles but distinct transport characteristics as auxins in plants. PAA is widely distributed in vascular and non-vascular plants. Although the biological activities of PAA are lower than those of IAA, the endogenous levels of PAA are much higher than those of IAA in various plant tissues in Arabidopsis. PAA and IAA can regulate the same set of auxin-responsive genes through the TIR1/AFB pathway in Arabidopsis. IAA actively forms concentration gradients in maize coleoptiles in response to gravitropic stimulation, whereas PAA does not, indicating that PAA is not actively transported in a polar manner. The induction of the YUCCA (YUC) genes increases PAA metabolite levels in Arabidopsis, indicating that YUC flavin-containing monooxygenases may play a role in PAA biosynthesis. Our results provide new insights into the regulation of plant growth and development by different types of auxins.

/pdf/distinct-characteristics-of-indole-3-acetic-acid-and-18a80ztfcu.pdf

Distinct Characteristics of Indole-3-Acetic Acid and Phenylacetic Acid, Two Common Auxins in Plants

Arabidopsis has three cytokinin receptors genes: CRE1, AHK2, and AHK3. Availability of plants that are homozygous mutant for these three genes indicates that cytokinin receptors in the haploid cells are dispensable for the development of male and female gametophytes. The triple mutants form a few flowers but never set seed, indicating that reproductive growth is impaired. We investigated which reproductive processes are affected in the triple mutants. Anthers of mutant plants contained fewer pollen grains and did not dehisce. Pollen in the anthers completed the formation of the one vegetative nucleus and the two sperm nuclei, as seen in wild type. The majority of the ovules were abnormal: 78% lacked the embryo sac, 10% carried a female gametophyte that terminated its development before completing three rounds of nuclear division, and about 12% completed three rounds of nuclear division but the gametophytes were smaller than those of the wild type. Reciprocal crosses between the wild type and the triple mu...

https://www.tandfonline.com/doi/pdf/10.4161/psb.6.1.13999

Kaori Kinoshita-Tsujimura

Papers

Cytokinins are central regulators of cambial activity

Distinct Characteristics of Indole-3-Acetic Acid and Phenylacetic Acid, Two Common Auxins in Plants

Cytokinin receptors in sporophytes are essential for male and female functions in Arabidopsis thaliana.

A Dof-CLE circuit controls phloem organization