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A Study on an ABC transporter that mediates the root-to-shoot translocation of cytokinin in Arabidopsis

A Study on an ABC transporter that mediates the root-to-shoot translocation of cytokinin in Arabidopsis
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Plants are composed of the aboveground structure, shoot, and the belowground structure, root. The shoot conducts photosynthesis and provides the products to the root via phloem, as building blocks and energy sources. On the other hand, the root absorbs water and minerals from soil and delivers them to the shoot through xylem. Therefore, the growth and activity of the two structures are tightly associated and need to be coordinated to adapt to the ever-changing environment; alteration in root growth or activity by changes in rhizosphere alters those of shoot and vice versa. This coordination is achieved by signal molecules which translocate between root and shoot to induce responses in the distant tissues under given envrionmental conditions. Cytokinin, a phytohormone, is one of the long-distance signal molecules transported from the site of biosynthesis to the distant tissues either via xylem or phloem. For example, cytokinins of N6-(Δ2-isopentenyl)adenine (iP) type are delivered from shoot to root via phloem and regulate vasculature patterning in root apical meristem. On the other hand, supply of nitrate to rhizosphere induces biosynthesis of trans-zeatin (tZ)-type cytokinins in the root and the hormone is translocated to the shoot via xylem. A recent study revealed that the root-derived tZ-type cytokinins stimulate shoot growth. However, the molecular identity underlying the long-distance transport of the cytokinin remained elusive. The aim of this study is to identify the transporter that mediates the root-to-shoot translocation of the cytokinin. To address the question, I hypothesized that the transporter would be expressed in spatiotemporally similar way with rate-limiting enzymes for cytokinin biosynthesis in the root. Therefore, I established the following three criteria to search for the candidate transporters using In silico database; (i) The transporter would be highly co-expressed with adenosine phosphate isopentenyltransferase 3, one of the most important enzymes for cytokinin biosynthesis; (ii) The transporter would be primarily expressed in root phloem companion cells where cytokinins are actively produced; (iii) The transporter would be up-regulated in transcription by cytokinin treatment. I screened transporters based on the criteria and found only one transporter, AtABCG14, which satisfied all the criteria. The high expression of the transporter in the cells synthesizing the cytokinins was confirmed by analysis of the AtABCG14 expression pattern in transgenic plants carrying reporter genes under the control of AtABCG14 promoter. The atabcg14 knockout mutant exhibited shoot growth retardation that was reminiscent of cytokinin-deficient mutants, but it was recovered by exogenously applied tZ. The results suggested that lack of tZ in the mutant shoot might cause the growth defects. As predicted, the content of tZ-type cytokinins in the mutant shoot was significantly decreased but increased in the mutant root compared to those of the wild type with the consistent changes in the expression level of cytokinin response genes. In addition, tZ-type cytokinins in the mutant xylem sap were dramatically reduced by ~90% compared to that of wild type, indicating that AtABCG14 plays crucial roles in the xylem loading and the acropetal transport of the cytokinins. Consistently, the translocation of 14C-labled tZ from root to shoot was significantly delayed in the mutant in comparison with the wild type. Grafting of atabcg14 scion onto the wild-type rootstock rescued the growth of the mutant shoot while the wild-type scion grafted on the mutant rootstock exhibited shoot growth defects. These results strongly indicate that AtABCG14 mediates the root-to-shoot translocation of cytokinin, which is important for the shoot growth. This study revealed the long-sought molecular identity for the acropetal transport of cytokinin. AtABCG14 is a first transporter, which showed physiological relevance by mediating the long-distance cytokinin transport. Therefore, this study provides new opportunities for investigating and manipulating the cytokinin-dependent pathways as well as cytokinin transport.
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