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Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions.

ABSTRACT: Dynamically polarized membrane proteins define different cell boundaries and have an important role in intercellular communication-a vital feature of multicellular development. Efflux carriers for the signalling molecule auxin from the PIN family are landmarks of cell polarity in plants and have a crucial involvement in auxin distribution-dependent development including embryo patterning, organogenesis and tropisms. Polar PIN localization determines the direction of intercellular auxin flow, yet the mechanisms generating PIN polarity remain unclear. Here we identify an endocytosis-dependent mechanism of PIN polarity generation and analyse its developmental implications. Real-time PIN tracking showed that after synthesis, PINs are initially delivered to the plasma membrane in a non-polar manner and their polarity is established by subsequent endocytic recycling. Interference with PIN endocytosis either by auxin or by manipulation of the Arabidopsis Rab5 GTPase pathway prevents PIN polarization. Failure of PIN polarization transiently alters asymmetric auxin distribution during embryogenesis and increases the local auxin response in apical embryo regions. This results in ectopic expression of auxin pathway-associated root-forming master regulators in embryonic leaves and promotes homeotic transformation of leaves to roots. Our results indicate a two-step mechanism for the generation of PIN polar localization and the essential role of endocytosis in this process. It also highlights the link between endocytosis-dependent polarity of individual cells and auxin distribution-dependent cell fate establishment for multicellular patterning.

SUBMITTER: Dhonukshe P

PROVIDER: S-EPMC2692841 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Background and aimsThe typical rootless linear shoots of aquatic carnivorous plants exhibit clear, steep polarity associated with very rapid apical shoot growth. The aim of this study was to determine how auxin and cytokinin contents are related to polarity and shoot growth in such plants.MethodsThe main auxin and cytokinin metabolites in separated shoot segments and turions of two carnivorous plants, Aldrovanda vesiculosa and Utricularia australis, were analysed using ultra-high-performance liquid chromatography coupled with triple quad mass spectrometry.Key resultsIn both species, only isoprenoid cytokinins were identified. Zeatin cytokinins predominated in the apical parts, with their concentrations decreasing basipetally, and the trans isomer predominated in A. vesiculosa whereas the cis form was more abundant in U australis. Isopentenyladenine-type cytokinins, in contrast, increased basipetally. Conjugated cytokinin metabolites, the O-glucosides, were present at high concentrations in A. vesiculosa but only in minute amounts in U. australis. N(9)-glucoside forms were detected only in U. australis, with isopentenyladenine-9-glucoside (iP9G) being most abundant. In addition to free indole-3-acetic acid (IAA), indole-3-acetamide (IAM), IAA-aspartate (IAAsp), IAA-glutamate (IAGlu) and IAA-glycine (IAGly) conjugates were identified.ConclusionsBoth species show common trends in auxin and cytokinin levels, the apical localization of the cytokinin biosynthesis and basipetal change in the ratio of active cytokinins to auxin, in favour of auxin. However, our detailed study of cytokinin metabolic profiles also revealed that both species developed different regulatory mechanisms of active cytokinin content; on the level of their degradation, in U. australis, or in the biosynthesis itself, in the case of A. vesiculosa Results indicate that the rapid turnover of these signalling molecules along the shoots is essential for maintaining the dynamic balance between the rapid polar growth and development of the apical parts and senescence of the older, basal parts of the shoots.

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Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions.

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