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AXR1 Acts After Lateral Bud Formation to Inhibit Lateral Bud Growth in Arabidopsis

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This is a repository copy of AXR1 acts after lateral bud formation to inhibit lateral bud growth in Arabidopsis. White Rose Research Online URL for this paper: https://eprints.whiterose.ac.uk/262/ Article: Stirnberg, P., Leyser, O. and Chatfield, S.P. (1999) AXR1 acts after lateral bud formation to inhibit lateral bud growth in Arabidopsis. Plant Physiology. pp. 839-847. ISSN 0032-0889 Reuse Items deposited in White Rose Research Online are protected by copyright, with all rights reserved unless indicated otherwise. They may be downloaded and/or printed for private study, or other acts as permitted by national copyright laws. The publisher or other rights holders may allow further reproduction and re-use of the full text version. This is indicated by the licence information on the White Rose Research Online record for the item. Takedown If you consider content in White Rose Research Online to be in breach of UK law, please notify us by emailing [email protected] including the URL of the record and the reason for the withdrawal request. [email protected] https://eprints.whiterose.ac.uk/ Plant Physiology, November 1999, Vol. 121, pp. 839–847, www.plantphysiol.org © 1999 American Society of Plant Physiologists AXR1 Acts after Lateral Bud Formation to Inhibit Lateral Bud Growth in Arabidopsis1 Petra Stirnberg, Steven P. Chatfield, and H.M. Ottoline Leyser* Department of Biology, University of York, P.O. Box 373, York YO10 5YW, United Kingdom Several mutants with altered auxin sensitivity have been The AXR1 gene of Arabidopsis is required for many auxin re- produced in Arabidopsis. One such locus, AXR1, is defined sponses. The highly branched shoot phenotype of mature axr1 by an allelic series of recessive mutations. The phenotype mutant plants has been taken as genetic evidence for a role of auxin of axr1 mutant plants is pleiotropic, with defects in root, in the control of shoot branching. We compared the development of hypocotyl, stamen, and stem elongation, vascular develop- lateral shoots in wild-type Columbia and axr1-12 plants. In the wild ment, lateral root formation, and root gravitropism. Leaf type, the pattern of lateral shoot development depends on the morphology is altered and shoot branching is increased at developmental stage of the plant. During prolonged vegetative maturity (Estelle and Somerville, 1987; Lincoln et al., 1990). growth, axillary shoots arise and develop in a basal-apical sequence. All axr1 tissues examined showed reduced auxin sensitiv- After floral transition, axillary shoots arise rapidly along the primary shoot axis and grow out to form lateral inflorescences in an apical- ity in a variety of assays, including rapid gene induction by basal sequence. For both patterns, the axr1 mutation does not affect auxin (Abel et al., 1995; Timpte et al., 1995). This suggests the timing of axillary meristem formation; however, subsequent that the AXR1 protein is required for auxin signaling. The lateral shoot development proceeds more rapidly in axr1 plants. The AXR1 gene encodes a protein related to the amino-terminal outgrowth of lateral inflorescences from excised cauline nodes of half of ubiquitin-activating enzyme; sequencing of severe wild-type plants is inhibited by apical auxin. axr1-12 nodes are mutant alleles such as axr1-12 indicates complete loss of resistant to this inhibition. These results provide evidence for com- protein function (Leyser et al., 1993). mon control of axillary growth in both patterns, and suggest a role Although these mutant and transgenic lines suggest that for auxin during the late stages of axillary shoot development branching is regulated by auxin in vivo, they were only following the formation of the axillary bud and several axillary leaf investigated at a cursory level. Altered branching may be primordia. an indirect consequence of other auxin-regulated pheno- types. axr1-12 plants produce more branches than the wild type, and are less fertile (Lincoln et al., 1990). There is In plants, the shoot apex has an inhibitory effect on the evidence that developing fruits limit lateral branching (Ta- development of lateral shoots. The theory that the plant mas et al., 1979; Hensel et al., 1994). Therefore, the in- hormone auxin (indole-3-acetic acid [IAA]) is a signal in creased branching in mature axr1 plants may be a conse- this apical dominance remains a matter of debate. This quence of their infertility. theory is based on the effects of auxin application on de- The in vivo role of auxin is further called into question by capitated plants and the discovery of basipetal auxin trans- examining the pattern of lateral shoot development in Ara- port. The mechanism by which auxin acts is still obscure bidopsis. If apically derived auxin acts as an inhibitor of and is likely to be indirect (see Phillips, 1975; Trewavas, axillary branching, one might expect the lateral buds clos- 1981; Cline, 1991, 1994). est to the shoot apex to be the most repressed, giving a The increasing number of mutations or transgenes that basal-apical (acropetal) sequence of bud growth. Arabidop- affect auxin content, transport, or sensitivity, especially in sis shows this pattern during prolonged vegetative growth, Arabidopsis, provides a different approach to investigate e.g. in late-flowering ecotypes (Grbic´and Bleecker, 1996). the role of auxin in apical dominance, and in particular However, lateral inflorescences develop in an apical-basal which stages of lateral shoot development it regulates in (basipetal) sequence after floral transition (Alvarez et al., vivo. Plants expressing the IAA biosynthetic genes from 1992; Hempel and Feldman, 1994). Agrobacterium tumefaciens have high endogenous IAA lev- To further assess the role of auxin in the regulation of els and increased apical dominance (Klee et al., 1987; Ro- Arabidopsis shoot branching, we compared axillary shoot mano et al., 1993, 1995). The iaaL gene from Pseudomonas development in the wild type and axr1-12 to determine the savastanoi, encoding an enzyme that conjugates IAA to Lys, earliest stage when differences can be detected. In addition, has been transformed into tobacco, resulting in reduced we compared the auxin sensitivity of wild-type and axr1-12 levels of free IAA and reduced apical dominance (Romano lateral inflorescence outgrowth using nodes excised from et al., 1991). the primary inflorescence. The axr1-12 mutation does not affect early stages of axillary shoot development; however, 1 This work was supported by a grant from the Biotechnology it promotes the subsequent growth of axillary shoots initi- and Biological Sciences Research Council of the United Kingdom. ated by the acropetal and basipetal pattern. It also renders * Corresponding author; e-mail [email protected]; fax the outgrowth of isolated lateral inflorescences resistant to 44–1904–434312. auxin inhibition. These results suggest a role for auxin in 839 840 Stirnberg et al. Plant Physiol. Vol. 121, 1999 the stages of lateral shoot development following axillary node with a visible axillary bud between parts of the apical meristem formation. and the basal internode and 8 to 15 mm long were excised from elongating primary inflorescences. The length of the bud was measured and the node was placed over the gap MATERIALS AND METHODS of a split plate, with the apical end inserted into one agar Plants for Morphometric and Histological Analyses half and the basal end into the other. Plates containing up to three excised nodes were incubated in the conditions Seeds of Arabidopsis (wild type and axr1-12, ecotype described above in near-vertical orientation. The lengths of Columbia) were sown onto F2 compost (Levington Horti- the axillary shoots were measured daily with a metric ruler culture, Ipswich, UK) in shallow trays consisting of indi- until d 8 following excision. Lengths were determined from ϫ vidual 4- 4-cm pots (P40, Cookson Plantpak, Maldon, the point where the adaxial side of the subtending petiole UK), with several seeds per pot. Compost for short-day- inserted into the stem to the tip of the axillary leaves when grown plants was treated with systemic insecticide (Inter- the bud was still closed, or to the inflorescence apex when cept 70WG, Levington Horticulture) before sowing. After 2 the branch had started elongating. to5dofcold treatment at 4°C, trays were transferred to 21°C, 8-h (short) or 16-h (long) photoperiods and watered Ϫ with tap water. Light intensities were 130 and 50 ␮mol m 2 Ϫ RESULTS s 1 for the short and long photoperiod, respectively. Seed- lings were thinned out to one per pot after germination. Development of the Branched Inflorescence in Long Photoperiods Histology To establish when differences in branching between axr1-12 and wild-type plants first arise, the development of Tissue was fixed overnight in 3% (v/v) formaldehyde/ their shoot systems was studied over time. Neither wild- 1.25% (v/v) glutaraldehyde in 0.05 m sodium phosphate type nor axr1-12 rosettes showed visible axillary buds or buffer (pH 7.0), dehydrated in a graded ethanol series, branches during vegetative growth in long photoperiods. transferred to Histoclear (National Diagnostics, Atlanta), After the transition to reproductive growth, flower buds and embedded in Paraplast Plus (Sigma-Aldrich, Poole, became visible in the center of the rosettes and the plants UK). Microtome sections (8 ␮m) were affixed to glass mi- started to bolt, as defined by visible elongation of the croscope slides covered with adhesive (1% [w/v] gelatin, lowermost internode of the primary inflorescence. The date 13% [v/v] glycerol), dewaxed in xylene, rehydrated in an of bolting was noted for each individual plant. Samples of ethanol series, stained in 0.025% (w/v) aqueous toluidine five to eight plants of each genotype were removed and blue, dehydrated in an ethanol series followed by xylene, subjected to morphometric analysis covering a time course and coverslips were mounted with DPX (BDH Laboratory of 3-d intervals between 3 and 18 d after bolting.
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