The plant signalling molecule auxin provides positional information in a variety of developmental processes by means of its differential distribution (gradients) within plant tissues. Thus, cellular auxin levels often determine the developmental output of auxin signalling. Conceptually, transmembrane transport and metabolic processes regulate the steady-state levels of auxin in any given cell. In particular, PIN auxin-efflux-carrier-mediated, directional transport between cells is crucial for generating auxin gradients. Here we show that Arabidopsis thaliana PIN5, an atypical member of the PIN gene family, encodes a functional auxin transporter that is required for auxin-mediated development. PIN5 does not have a direct role in cell-to-cell transport but regulates intracellular auxin homeostasis and metabolism. PIN5 localizes, unlike other characterized plasma membrane PIN proteins, to endoplasmic reticulum (ER), presumably mediating auxin flow from the cytosol to the lumen of the ER. The ER localization of other PIN5-like transporters (including the moss PIN) indicates that the diversification of PIN protein functions in mediating auxin homeostasis at the ER, and cell-to-cell auxin transport at the plasma membrane, represent an ancient event during the evolution of land plants.
The phytohormone auxin acts as a prominent signal, providing, by its local accumulation or depletion in selected cells, a spatial and temporal reference for changes in the developmental program [1][2][3][4][5][6][7] . The distribution of auxin depends on both auxin metabolism (biosynthesis, conjugation and degradation) [8][9][10] and cellular auxin transport [11][12][13][14][15] . We identified in silico a novel putative auxin transport facilitator family, called PIN-LIKES (PILS). Here we illustrate that PILS proteins are required for auxin-dependent regulation of plant growth by determining the cellular sensitivity to auxin. PILS proteins regulate intracellular auxin accumulation at the endoplasmic reticulum and thus auxin availability for nuclear auxin signalling. PILS activity affects the level of endogenous auxin indole-3-acetic acid (IAA), presumably via intracellular accumulation and metabolism. Our findings reveal that the transport machinery to compartmentalize auxin within the cell is of an unexpected molecular complexity and demonstrate this compartmentalization to be functionally important for a number of developmental processes.Prominent auxin carriers with fundamental importance during plant development are PIN-FORMED (PIN) proteins [1][2][3]6,9,15 . PIN1-type auxin carriers regulate the directional intercellular auxin transport at the plasma membrane. In contrast, atypical family member PIN5 regulates intracellular auxin compartmentalization into the lumen of the endoplasmic reticulum and its role in auxin homeostasis was recently identified 15,16 . PIN proteins have a predicted central hydrophilic loop, flanked at each side by five transmembrane domains. We screened in silico for novel PIN-like putative carrier proteins with a predicted topology similar to PIN proteins ( Fig. 1a and Supplementary Fig. 2) and identified a protein family of seven members (Fig. 1b) in Arabidopsis thaliana, which we designated as the PILS proteins. In contrast to the similarities in the predicted protein topology, PIN and PILS proteins do not show pronounced protein sequence identity (10-18%), which limits the identification of PILS proteins by conventional, reciprocal basic local alignment search tool (BLAST) approaches. However, the distinct PIN and PILS protein families contain both the InterPro auxin carrier domain which is an insilico-defined domain, aiming to predict auxin transport function (http://www.ebi.ac.uk/panda/InterPro.html). The PILS putative carrier family is conserved throughout the whole plant lineage, including unicellular algae (such as Ostreococcus tauri and Chlamydomonas reinhardtii) (Supplementary Fig. 3) where PIN proteins are absent 16 , indicating that PILS proteins are evolutionarily older.PILS genes are broadly expressed in various tissues (Fig. 1c) and PILS2-PILS7 were transcriptionally upregulated by auxin application in wild-type seedlings (Fig. 1d-f and Supplementary Fig. 4), indicating a role in auxin-dependent processes. To investigate the potential function of the putative PILS auxi...
Cytokinins (CKs) are plant hormones affecting numerous developmental processes. Zeatin and its derivatives are the most important group of isoprenoid CKs. Zeatin occurs as two isomers: while trans-zeatin (transZ) was found to be a bioactive substance, cis-zeatin (cisZ) was reported to have a weak biological impact. Even though cisZ derivatives are abundant in various plant materials their biological role is still unknown. The comprehensive screen of land plants presented here suggests that cisZ-type CKs occur ubiquitously in the plant kingdom but their abundance might correlate with a strategy of life rather than with evolutionary complexity. Changing levels of transZ and cisZ during Arabidopsis ontogenesis show that levels of the two zeatin isomers can differ significantly during the life span of the plant, with cisZ-type CKs prevalent in the developmental stages associated with limited growth. A survey of the bioassays employed illustrates mild activity of cisZ and its derivatives. No cis↔trans isomerization, which would account for the effects of cisZ, was observed in tobacco cells and oat leaves. Differences in uptake between the two isomers resulting in distinct bioactivity have not been detected. In contrast, cisZ and transZ have a different metabolic fate in oat and tobacco. Analysis of a CK-degrading enzyme, cytokinin oxidase/dehydrogenase (CKX), reveals that Arabidopsis possesses two isoforms, AtCKX1 expressed in stages of active growth, and AtCKX7, both of which have the highest affinity for the cisZ isomer. Based on the present results, the conceivable function of cisZ-type CKs as delicate regulators of CK responses in plants under growth-limiting conditions is hypothesized.
The bacterial quorum sensing signals N-acyl-L: -homoserine lactones enable bacterial cells to regulate gene expression depending on population density, in order to undertake collective actions such as the infection of host cells. Only little is known about the molecular ways of plants reacting to these bacterial signals. In this study we show that the contact of Arabidopsis thaliana roots with N-hexanoyl-DL: -homoserine-lactone (C6-HSL) resulted in distinct transcriptional changes in roots and shoots, respectively. Interestingly, unlike most other bacterial signals, C6-HSL influenced only a few defense-related transcripts. Instead, several genes associated with cell growth as well as genes regulated by growth hormones showed changes in their expression after C6-HSL treatment. C6-HSL did not induce plant systemic resistance against Pseudomonas syringae. The inoculation of roots with different types of AHLs led predominantly for short chain N-butyryl-DL: -homoserine lactone and C6-HSL to root elongation. Determination of plant hormone concentrations in root and shoot tissues supported alterations of auxin to cytokinin ratio. Finally, we provide evidence that Arabidopsis takes up bacterial C6-HSL and allows systemic distribution throughout the plant. In sum, the bacterial quorum sensing signal C6-HSL does induce transcriptional changes in Arabidopsis and may contribute to tuning plant growth to the microbial composition of the rhizosphere.
Heterodera schachtii, a plant-parasitic cyst nematode, invades host roots and induces a specific syncytial feeding structure, from which it withdraws all required nutrients, causing severe yield losses. The system H. schachtii–Arabidopsis is an excellent research model for investigating plant defence mechanisms. Such responses are suppressed in well-established syncytia, whereas they are induced during early parasitism. However, the mechanisms by which the defence responses are modulated and the role of phytohormones are largely unknown. The aim of this study was to elucidate the role of hormone-based defence responses at the onset of nematode infection. First, concentrations of main phytohormones were quantified and the expression of several hormone-related genes was analysed using quantitative real-time (qRT)-PCR or GeneChip. Further, the effects of individual hormones were evaluated via nematode attraction and infection assays using plants with altered endogenous hormone concentrations. Our results suggest a pivotal and positive role for ethylene during nematode attraction, whereas jasmonic acid triggers early defence responses against H. schachtii. Salicylic acid seems to be a negative regulator during later syncytium and female development. We conclude that nematodes are able to impose specific changes in hormone pools, thus modulating hormone-based defence and signal transduction in strict dependence on their parasitism stage.
Polar auxin transport (PAT) plays key roles in the regulation of plant growth and development. Flavonoids have been implicated in the inhibition of PAT. However, the active flavonoid derivative(s) involved in this process in vivo has not yet been identified. Here, we provide evidence that a specific flavonol bis-glycoside is correlated with shorter plant stature and reduced PAT.Specific flavonoid-biosynthetic or flavonoid-glycosylating steps were genetically blocked in Arabidopsis thaliana. The differential flavonol patterns established were analyzed by high-performance liquid chromatography (HPLC) and related to altered plant stature. PAT was monitored in stem segments using a radioactive [3H]-indole-3-acetic acid tracer.The flavonoid 3-O-glucosyltransferase mutant ugt78d2 exhibited a dwarf stature in addition to its altered flavonol glycoside pattern. This was accompanied by reduced PAT in ugt78d2 shoots. The ugt78d2-dependent growth defects were flavonoid dependent, as they were rescued by genetic blocking of flavonoid biosynthesis. Phenotypic and metabolic analyses of a series of mutants defective at various steps of flavonoid formation narrowed down the potentially active moiety to kaempferol 3-O-rhamnoside-7-O-rhamnoside. Moreover, the level of this compound was negatively correlated with basipetal auxin transport.These results indicate that kaempferol 3-O-rhamnoside-7-O-rhamnoside acts as an endogenous PAT inhibitor in Arabidopsis shoots.
Transgenerational effects might play an important role in the clonal plant Trifolium repens and are probably mediated by epigenetic variation. The growth and behavior of clonal plants might be affected not only by the ambient environment but also by environments that are no longer present at the time of clonal reproduction. This phenomenon can have yet unacknowledged ecological and evolutionary implications for clonal plants.
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