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      Ontogenetic Changes in Auxin Biosynthesis and Distribution Determine the Organogenic Activity of the Shoot Apical Meristem in pin1 Mutants

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          Abstract

          In the shoot apical meristem (SAM) of Arabidopsis, PIN1-dependent polar auxin transport (PAT) regulates two crucial developmental processes: organogenesis and vascular system formation. However, the knockout mutation in the PIN1 gene does not fully inhibit these two processes. Therefore, we investigated a potential source of auxin for organogenesis and vascularization during inflorescence stem development. We analyzed auxin distribution in wild-type (WT) and pin1 mutant plants using a refined protocol of auxin immunolocalization; auxin activity, with the response reporter pDR5:GFP; and expression of auxin biosynthesis genes YUC1 and YUC4. Our results revealed that regardless of the functionality of PIN1-mediated PAT, auxin is present in the SAM and vascular strands. In WT plants, auxin always accumulates in all cells of the SAM, whereas in pin1 mutants, its localization within the SAM changes ontogenetically and is related to changes in the structure of the vascular system, organogenic activity of SAM, and expression levels of YUC1 and YUC4 genes. Our findings indicate that the presence of auxin in the meristem of pin1 mutants is an outcome of at least two PIN1-independent mechanisms: acropetal auxin transport from differentiated tissues with the use of vascular strands and auxin biosynthesis within the SAM.

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          Local, efflux-dependent auxin gradients as a common module for plant organ formation.

          Plants, compared to animals, exhibit an amazing adaptability and plasticity in their development. This is largely dependent on the ability of plants to form new organs, such as lateral roots, leaves, and flowers during postembryonic development. Organ primordia develop from founder cell populations into organs by coordinated cell division and differentiation. Here, we show that organ formation in Arabidopsis involves dynamic gradients of the signaling molecule auxin with maxima at the primordia tips. These gradients are mediated by cellular efflux requiring asymmetrically localized PIN proteins, which represent a functionally redundant network for auxin distribution in both aerial and underground organs. PIN1 polar localization undergoes a dynamic rearrangement, which correlates with establishment of auxin gradients and primordium development. Our results suggest that PIN-dependent, local auxin gradients represent a common module for formation of all plant organs, regardless of their mature morphology or developmental origin.
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            TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development.

            Plants have evolved a tremendous ability to respond to environmental changes by adapting their growth and development. The interaction between hormonal and developmental signals is a critical mechanism in the generation of this enormous plasticity. A good example is the response to the hormone ethylene that depends on tissue type, developmental stage, and environmental conditions. By characterizing the Arabidopsis wei8 mutant, we have found that a small family of genes mediates tissue-specific responses to ethylene. Biochemical studies revealed that WEI8 encodes a long-anticipated tryptophan aminotransferase, TAA1, in the essential, yet genetically uncharacterized, indole-3-pyruvic acid (IPA) branch of the auxin biosynthetic pathway. Analysis of TAA1 and its paralogues revealed a link between local auxin production, tissue-specific ethylene effects, and organ development. Thus, the IPA route of auxin production is key to generating robust auxin gradients in response to environmental and developmental cues.
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              Auxin transport routes in plant development.

              The differential distribution of the plant signaling molecule auxin is required for many aspects of plant development. Local auxin maxima and gradients arise as a result of local auxin metabolism and, predominantly, from directional cell-to-cell transport. In this primer, we discuss how the coordinated activity of several auxin influx and efflux systems, which transport auxin across the plasma membrane, mediates directional auxin flow. This activity crucially contributes to the correct setting of developmental cues in embryogenesis, organogenesis, vascular tissue formation and directional growth in response to environmental stimuli.
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                Author and article information

                Journal
                Int J Mol Sci
                Int J Mol Sci
                ijms
                International Journal of Molecular Sciences
                MDPI
                1422-0067
                06 January 2019
                January 2019
                : 20
                : 1
                : 180
                Affiliations
                Department of Plant Developmental Biology, Institute of Experimental Biology, Faculty of Biological Sciences, University of Wroclaw, Kanonia 6/8, 50-328 Wroclaw, Poland; magdalena.biedron@ 123456uwr.edu.pl (M.B.); alicja.dolzblasz@ 123456uwr.edu.pl (A.D.); mateusz.berezowski@ 123456uwr.edu.pl (M.A.B.)
                Author notes
                [* ]Correspondence: alicja.banasiak@ 123456uwr.edu.pl ; Tel.: +48-71-375-4093
                [†]

                Current address: Department of Genetics and Cellular Physiology, Institute of Experimental Biology, Faculty of Biological Sciences, University of Wroclaw, Kanonia 6/8, 50-328 Wroclaw, Poland.

                Author information
                https://orcid.org/0000-0002-9540-4694
                Article
                ijms-20-00180
                10.3390/ijms20010180
                6337202
                30621327
                226ef423-fdfc-4256-ad2d-dd6694defa4f
                © 2019 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 19 November 2018
                : 02 January 2019
                Categories
                Article

                Molecular biology
                arabidopsis,auxin immunolocalization,organogenesis,pat,pin1 mutant,yuc genes,sam,vascular system,xylem

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