The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport

BACKGROUND: Plants achieve remarkable plasticity in shoot system architecture by regulating the activity of secondary shoot meristems, laid down in the axil of each leaf. Axillary meristem activity, and hence shoot branching, is regulated by a network of interacting hormonal signals that move through the plant. Among these, auxin, moving down the plant in the main stem, indirectly inhibits axillary bud outgrowth, and an as yet undefined hormone, the synthesis of which in Arabidopsis requires MAX1, MAX3, and MAX4, moves up the plant and also inhibits shoot branching. Since the axillary buds of max4 mutants are resistant to the inhibitory effects of apically supplied auxin, auxin and the MAX-dependent hormone must interact to inhibit branching. RESULTS: Here we show that the resistance of max mutant buds to apically supplied auxin is largely independent of the known, AXR1-mediated, auxin signal transduction pathway. Instead, it is caused by increased capacity for auxin transport in max primary stems, which show increased expression of PIN auxin efflux facilitators. The max phenotype is dependent on PIN1 activity, but it is independent of flavonoids, which are known regulators of PIN-dependent auxin transport. CONCLUSIONS: The MAX-dependent hormone is a novel regulator of auxin transport. Modulation of auxin transport in the stem is sufficient to regulate bud outgrowth, independent of AXR1-mediated auxin signaling. We therefore propose an additional mechanism for long-range signaling by auxin in which bud growth is regulated by competition between auxin sources for auxin transport capacity in the primary stem.     

MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone

The plant shoot body plan is highly variable, depending on the degree of branching. Characterization of the max1-max4 mutants of Arabidopsis demonstrates that branching is regulated by at least one carotenoid-derived hormone. Here we show that all four MAX genes act in a single pathway, with MAX1, MAX3, and MAX4 acting in hormone synthesis, and MAX2 acting in perception. We propose that MAX1 acts on a mobile substrate, downstream of MAX3 and MAX4, which have immobile substrates. These roles for MAX3, MAX4, and MAX2 are consistent with their known molecular identities. We identify MAX1 as a member of the cytochrome P450 family with high similarity to mammalian Thromboxane A2 synthase. This, with its expression pattern, supports its suggested role in the MAX pathway. Moreover, the proposed enzymatic series for MAX hormone synthesis resembles that of two already characterized signal biosynthetic pathways: prostaglandins in animals and oxilipins in plants.     

植物茎分枝的分子调控

植物茎分枝结构决定了不同植物的不同形态结构.本文从腋生分生组织的发生、腋芽的生长两个方面综述了近年来植物分枝发生发育相关的分子机理研究及其进展.发现在不同植物中腋分生组织形成的基本机制是相似的,LS（lateral suppressor）及其同源基因在不同植物中都参与腋生分生组织的形成,而BL(blind)及其同源基因也参与调控腋生分生组织的形成.腋生分生组织的形成可能也是受激素调控的.目前,对腋芽生长的分子调控机制的认识主要集中于生长素通过二级信使的作用调控腋芽的生长.而生长素调控腋芽生长的机制已经较为清楚的有两条途径：一是生长素通过抑制细胞分裂素合成来调控腋芽的生长;另一途径是一种类胡萝卜素衍生的信号物质参与生长素的运输调控(MAX途径)来调控腋芽的生长.最新研究表明,TB1的拟南芥同源基因在MAX途径的下游负调控腋芽的生长.此外,增强表达OsNAC2也促进腋芽的生长.     

Regulation of Shoot and Root Development through Mutual Signaling

Plants adjust their development in relation to the availability of nutrient sources. This necessitates signaling between root and shoot. Aside from the well-known systemic signaling processes mediated by auxin, cytokinin, and sugars, new pathways involving carotenoid-derived hormones have recently been identified. The auxin-responsive MAX pathway controls shoot branching through the biosynthesis of strigolactone in the roots. The BYPASS1 gene affects the production of an as-yet unknown carotenoid-derived substance in roots that promotes shoot development. Novel local and systemic mechanisms that control adaptive root development in response to nitrogen and phosphorus starvation were recently discovered. Notably, the ability of the NITRATE TRANSPORTER 1.1 to transport auxin drew for the first time a functional link between auxin, root development, and nitrate availability in soil. The study of plant response to phosphorus starvation allowed the identification of a systemic mobile miRNA. Deciphering and integrating these signaling pathways at the whole-plant level provide a new perspective for understanding how plants regulate their development in response to environmental cues.     

Strigolactones and shoot branching: a new trick for a young dog

Strigolactones secreted by plant roots are exploited by parasitic plants as germination triggers, making their synthesis and signaling important targets for crop protection. Meanwhile, genetic analyses have identified several genes required for the synthesis and signaling of an unknown shoot branching inhibitor. Two recent papers unite these two fields, showing that strigolactones control shoot branching.     

Plant signaling: notes from the underground

New studies combining genetic and grafting approaches in Arabidopsis provide evidence that a carotenoid derivative is a novel plant signaling molecule through which roots can influence shoot branching and leaf development.     

Characterization of MORE AXILLARY GROWTH Genes in Populus

Background

Strigolactones are a new class of plant hormones that play a key role in regulating shoot branching. Studies of branching mutants in Arabidopsis, pea, rice and petunia have identified several key genes involved in strigolactone biosynthesis or signaling pathway. In the model plant Arabidopsis, MORE AXILLARY GROWTH1 (MAX1), MAX2, MAX3 and MAX4 are four founding members of strigolactone pathway genes. However, little is known about the strigolactone pathway genes in the woody perennial plants.

Methodology/Principal Finding

Here we report the identification of MAX homologues in the woody model plant Populus trichocarpa. We identified the sequence homologues for each MAX protein in P. trichocarpa. Gene expression analysis revealed that Populus MAX paralogous genes are differentially expressed across various tissues and organs. Furthermore, we showed that Populus MAX genes could complement or partially complement the shoot branching phenotypes of the corresponding Arabidopsis max mutants.

Conclusion/Significance

This study provides genetic evidence that strigolactone pathway genes are likely conserved in the woody perennial plants and lays a foundation for further characterization of strigolactone pathway and its functions in the woody perennial plants.     

生长素调控植物株型形成的研究进展

高等植物通过调节顶端分生组织和侧生分生组织的活性建立地上株型系统,分生组织的活性受环境信号、发育阶段和遗传因素的综合调控,植物激素参与这些信号的整合。顶端优势是植物分枝调控的核心问题,而生长素对顶端优势的形成和维持发挥关键作用。本文综述了近几年与植物地上部分株型形成相关的生长素合成代谢、极性运输及信号转导领域的研究进展,并提出了展望。     

生长素调控植物株型形成的研究进展

高等植物通过调节顶端分生组织和侧生分生组织的活性建立地上株型系统, 分生组织的活性受环境信号、发育阶段和遗传因素的综合调控, 植物激素参与这些信号的整合。顶端优势是植物分枝调控的核心问题, 而生长素对顶端优势的形成和维持发挥关键作用。本文综述了近几年与植物地上部分株型形成相关的生长素合成代谢、极性运输及信号转导领域的研究进展, 并提出了展望。     

Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis

Karrikins are butenolides derived from burnt vegetation that stimulate seed germination and enhance seedling responses to light. Strigolactones are endogenous butenolide hormones that regulate shoot and root architecture, and stimulate the branching of arbuscular mycorrhizal fungi. Thus, karrikins and strigolactones are structurally similar but physiologically distinct plant growth regulators. In Arabidopsis thaliana, responses to both classes of butenolides require the F-box protein MAX2, but it remains unclear how discrete responses to karrikins and strigolactones are achieved. In rice, the DWARF14 protein is required for strigolactone-dependent inhibition of shoot branching. Here, we show that the Arabidopsis DWARF14 orthologue, AtD14, is also necessary for normal strigolactone responses in seedlings and adult plants. However, the AtD14 paralogue KARRIKIN INSENSITIVE 2 (KAI2) is specifically required for responses to karrikins, and not to strigolactones. Phylogenetic analysis indicates that KAI2 is ancestral and that AtD14 functional specialisation has evolved subsequently. Atd14 and kai2 mutants exhibit distinct subsets of max2 phenotypes, and expression patterns of AtD14 and KAI2 are consistent with the capacity to respond to either strigolactones or karrikins at different stages of plant development. We propose that AtD14 and KAI2 define a class of proteins that permit the separate regulation of karrikin and strigolactone signalling by MAX2. Our results support the existence of an endogenous, butenolide-based signalling mechanism that is distinct from the strigolactone pathway, providing a molecular basis for the adaptive response of plants to smoke.     

Strigolactone Promotes Degradation of DWARF14, an α/β Hydrolase Essential for Strigolactone Signaling in Arabidopsis

Strigolactones (SLs) are phytohormones that play a central role in regulating shoot branching. SL perception and signaling involves the F-box protein MAX2 and the hydrolase DWARF14 (D14), proposed to act as an SL receptor. We used strong loss-of-function alleles of the Arabidopsis thaliana D14 gene to characterize D14 function from early axillary bud development through to lateral shoot outgrowth and demonstrated a role of this gene in the control of flowering time. Our data show that D14 distribution in vivo overlaps with that reported for MAX2 at both the tissue and subcellular levels, allowing physical interactions between these proteins. Our grafting studies indicate that neither D14 mRNA nor the protein move over a long range upwards in the plant. Like MAX2, D14 is required locally in the aerial part of the plant to suppress shoot branching. We also identified a mechanism of SL-induced, MAX2-dependent proteasome-mediated degradation of D14. This negative feedback loop would cause a substantial drop in SL perception, which would effectively limit SL signaling duration and intensity.     

Strigolactones are a new-defined class of plant hormones which inhibit shoot branching and mediate the interaction of plant-AM fungi and plant-parasitic weeds

Because plants are sessile organisms, the ability to adapt to a wide range of environmental conditions is critical for their survival. As a consequence, plants use hormones to regulate growth, mitigate biotic and abiotic stresses, and to communicate with other organisms. Many plant hormones function plei-otropically in vivo, and often work in tandem with other hormones that are chemically distinct. A newly-defined class of plant hormones, the strigolactones, cooperate with auxins and cytokinins to control shoot branching and the outgrowth of lateral buds. Strigolactones were originally identified as compounds that stimulated the germination of parasitic plant seeds, and were also demonstrated to induce hyphal branching in arbuscular mycorrhizal (AM) fungi. AM fungi form symbioses with higher plant roots and mainly facilitate the absorption of phosphate from the soil. Conforming to the classical definition of a plant hormone, strigolactones are produced in the roots and translocated to the shoots where they inhibit shoot outgrowth and branching. The biosynthesis of this class of compounds is regulated by soil nutrient availability, i.e. the plant will increase its production of strigolactones when the soil phosphate concentration is limited, and decrease production when phosphates are in ample supply. Strigolactones that affect plant shoot branching, AM fungal hyphal branching, and seed ger-mination in parasitic plants facilitate chemical synthesis of similar compounds to control these and other biological processes by exogenous application.     

拟南芥MAX2蛋白功能研究进展

独角金内酯(strigolactone, SLs)是一类新型植物激素,在植物生长发育的进程中发挥多种重要功能,包括调控植物的分枝,促进种子的萌发,以及影响根系建成等。MAX2 (more axillary growth 2)是SL信号传导途径的关键调控因子,位于合成途径基因MAX1、MAX3和MAX4的下游,几乎影响独脚金内酯所控制的所有表型。近年来,MAX2多样化的功能逐步得到揭示,大量数据表明MAX2不仅仅是SL信号的重要组分,同时也参与SL和多种激素信号间的交叉互作,在植物生长发育的各个环节,以及抵御生物和非生物胁迫的反应中都发挥至关重要的作用,但具体调控机制还有待更加深入的研究。对目前已知的MAX2功能进行了总结和阐述,以期为全面揭示MAX2功能及其调控多种激素信号的交叉机制提供理论参考。     

Shoot branching

The mature form of a plant shoot system is an expression of several genetically controlled traits, many of which are also environmentally regulated. A major component of this architectural variation is the degree of shoot branching. Recent results indicate conserved mechanisms for shoot branch development across the monocots and eudicots. The existence of a novel long-range branch-inhibiting signal has been inferred from studies of branching mutants in pea and Arabidopsis.     

Connective Auxin Transport in the Shoot Facilitates Communication between Shoot Apices

The bulk polar movement of the plant signaling molecule auxin through the stem is a long-recognized but poorly understood phenomenon. Here we show that the highly polar, high conductance polar auxin transport stream (PATS) is only part of a multimodal auxin transport network in the stem. The dynamics of auxin movement through stems are inconsistent with a single polar transport regime and instead suggest widespread low conductance, less polar auxin transport in the stem, which we term connective auxin transport (CAT). The bidirectional movement of auxin between the PATS and the surrounding tissues, mediated by CAT, can explain the complex auxin transport kinetics we observe. We show that the auxin efflux carriers PIN3, PIN4, and PIN7 are major contributors to this auxin transport connectivity and that their activity is important for communication between shoot apices in the regulation of shoot branching. We propose that the PATS provides a long-range, consolidated stream of information throughout the plant, while CAT acts locally, allowing tissues to modulate and be modulated by information in the PATS.