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The BUD2 Mutation Affects Plant Architecture Through Altering Cytokinin and Auxin Responses in Arabidopsis

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The BUD2 Mutation Affects Plant Architecture Through Altering Cytokinin and Auxin Responses in Arabidopsis npg Polyamines, cytokinin, auxin and branching Cell Research (2010) 20:576-586. 576 © 2010 IBCB, SIBS, CAS All rights reserved 1001-0602/10 $ 32.00 npg ORIGINAL ARTICLE www.nature.com/cr The BUD2 mutation affects plant architecture through altering cytokinin and auxin responses in Arabidopsis Xia Cui1, *, Chunmin Ge1, 3, *, Renxiao Wang1, 4, Huanzhong Wang1, 5, Weiqi Chen2, Zhiming Fu1, Xiangning Jiang2, Jiayang Li1, Yonghong Wang1 1State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China; 2The Tree and Ornamental Plant Breeding and Biotechnology Lab- oratory of State Forestry Administration, College of Life Sciences and Biotechnology, Beijing Forestry University, Beijing 100083, China The ratio of auxin and cytokinin plays a crucial role in regulating aerial architecture by promoting or repressing axillary bud outgrowth. We have previously identified an Arabidopsis mutant bud2 that displays altered root and shoot architecture, which results from the loss-of-function of S-adenosylmethionine decarboxylase 4 (SAMDC4). In this study, we demonstrate that BUD2 could be induced by auxin, and the induction is dependent on auxin signaling. The mutation of BUD2 results in hyposensitivity to auxin and hypersensitivity to cytokinin, which is confirmed by callus induction assays. Our study suggests that polyamines may play their roles in regulating the plant architecture through affecting the homeostasis of cytokinins and sensitivities to auxin and cytokinin. Keywords: BUD2, shoot branching, auxin, cytokinin Cell Research (2010) 20:576-586. doi:10.1038/cr.2010.51; published online 13 April 2010 Introduction height or more branches in shoots and roots [4, 10-13]. However, the underlying mechanisms still remain largely Polyamines, including diamine putrescine, triamine elusive. spermidine and tetraamine spermine, are low-molecular- Branches of higher plants originate from the axillary mass organic cations. They exist widely in all living meristems (AMs) of shoots, and formation of a branch organisms and are essential for their survival, because generally consists of the initiation of a new AM and its blocking of the biosynthesis of polyamines leads to le- subsequent outgrowth. However, an AM may arrest its thal phenotypes in animals [1] and higher plants [2-4]. In growth under some conditions, forming a dormant bud. higher plants, polyamines have been proposed to func- The dormant buds will release their outgrowth once they tion in response to environmental stresses and in regu- sense a permissible environmental or developmental sig- lating growth and development [4-11]. Plant molecular nal. In many plant species, axillary buds become dormant and physiological studies over past decades have shown due to the inhibiting effects of the primary shoot apex on that higher plants defective in producing polyamines the outgrowth of AMs, a phenomenon known as ‘apical often have altered plant architecture, with reduced plant dominance’. Auxin was first regarded as a direct regula- tor in this process [14], a notion strengthened thereafter by physiological studies on decapitated shoot apices [15- *These two authors contributed equally to this work. 17], and by analyzing auxin biosynthesis, transport and Correspondence: Yonghong Wang Tel: +86-10-64806008; Fax: +86-10-64883428 signaling [18-29] in plants. However, when radiolabelled E-mail: [email protected] auxin was applied to a decapitated stump, the outgrowth 3Current address: The Stowers Institute for Medical Research, Kansas, of axillary buds was inhibited even though radiolabelled 4 USA. Current address: Institute of Biology II, Albert Ludwigs University, auxin was not found to accumulate in axillary buds, sug- Freiburg, Germany. 5Current address: The Samuel Roberts Noble Founda- tion, Ardmore, USA. gesting an indirect suppression effect of auxin on the AM Received 1 September 2009; revised 30 November 2009; accepted 26 outgrowth [28, 30] and the presence of second messen- January 2010, published online 13 April 2010 gers. Cell Research | Vol 20 No 5 | May 2010 Xia Cui et al. npg 577 Cytokinin has been proposed as a second messenger A 20 ºC 29 ºC that mediates the action of auxin in controlling the apical dominance, because it promotes the outgrowth of lateral buds when directly applied to buds [31]. Although an an- tagonistic role of auxin and cytokinin in the regulation of apical dominance has been postulated for decades, little is known about the underlying molecular mechanisms. Recent studies have shown that auxin can regulate the WT bud2-2 WT bud2-2 expressions of IPT genes and that cytokinin biosynthesis is directly affected by auxin in local shoots [32, 33], sug- B gesting that auxin may modulate cytokinin concentration 80 and thus represses AM outgrowth [31, 34-36]. WT WT-De Recent studies on a series of branching mutants, such 60 bud2-2 bud2-2-De as more axillary growth (max) of Arabidopsis [37-40], ramosus (rms) mutants of pea [41-43], decreased apical dominance (dad) mutants of petunia [44, 45] and dwarf 40 (d) mutants of rice [46-51], have revealed strigolactone as a second messenger of auxin action on the control of 20 AM outgrowth [52, 53]. Strigolactones, a group of ter- Length of bud outgrowth (mm) penoid lactones that have been found in root exudates of 0 diverse plant species, are synthesized from carotenoids in 0 1 2 3 4 5 6 7 8 9 roots and transported acropetally or synthesized locally Days after decapitation to repress the outgrowth of shoot branches [38, 54-56]. Figure 1 Hypocotyl elongation at high temperature and branch- However, the biosynthesis and signaling pathways still ing of decapitated plants. (A) Induction of hypocotyl elongation remain to be elucidated. by high temperature. Wild-type and bud2 mutant seedlings were Moreover, polyamines have been demonstrated to grown on 1/2 MS plates at 20 °C or 29 °C for 9 days and photo- play a regulatory role in controlling the outgrowth of ax- graphed at the same magnification. (B) The growth rate of the illary buds in the Arabidopsis mutant, bushy and dwarf lowest cauline bud in intact and decapitated plants. The lowest 2 (bud2) [4], which shows a dwarf and bushy pheno- cauline bud length of the intact and decapitated plants (decapi- type. The BUD2 gene encodes S-adenosylmethionine tated above the lowest cauline bud 1.0 cm) were measured ev- ery 24 h until day 9. Error bars show SE (n = 5). decarboxylase 4 (SAMDC4), an enzyme required for the biosynthesis of polyamines in Arabidopsis thaliana. In this study, we show that polyamines may play their roles in regulating the plant architecture through affecting the 9-day-old bud2 seedlings grown at 29 °C was seriously homeostasis of cytokinins and sensitivities to auxin and inhibited compared with that of the wild-type seedlings, cytokinin. suggesting that bud2 may have an altered auxin-depen- dent developmental process. This was further strength- Results ened by the decapitation experiment. As shown in Figure 1B, the outgrowth rate of lateral buds of decapitated The bud2 plant shows altered hypocotyl elongation and wild-type plants was significantly accelerated compared lateral bud outgrowth with that of the decapitated bud2 plants, indicating that Our previous study showed that the bushy and dwarf the bud2 plant has an abnormal response to shoot decapi- phenotype of the Arabidopsis bud2 mutant plant results tation. These results strongly suggest that the bud2 mu- from the defect in the biosynthesis of polyamines [4]. To tant plant has an altered auxin-related development. investigate whether the loss of apical dominance of bud2 plants involves auxin action, we examined the hypocotyl The bud2 plant is hyposensitive to exogenous auxin elongation at higher temperature and the lateral shoot To determine whether the biosynthesis, transport or development after decapitation of wild-type and bud2 signaling of auxin is altered in the bud2 mutant plant, mutant plants [43, 57, 58]. Identification of temperature- we compared the IAA concentration, polar auxin trans- induced hypocotyl elongation is a simple and rapid as- port (PAT) and response to auxin between the wild- say in the study of an auxin-mediated growth response type and mutant plants. No significant differences in [59]. As shown in Figure 1A, the hypocotyl length of the the IAA contents of seedlings and the PAT capacity of www.cell-research.com | Cell Research npg Polyamines, cytokinin, auxin and branching 578 roots and inflorescence stems were found between bud2 to exogenous auxin, suggesting that polyamines may be and wild-type plants (see Supplementary information, involved in regulating root and shoot branching through Figures S1 and S2). However, application of a low con- affecting auxin response in Arabidopsis. Consistently, we centration of exogenous auxin (1.0 nM 1-naphthalene found that the expression levels of primary auxin-respon- acetic acid, NAA) to bud2 seedlings showed no effect sive genes, IAA1 and IAA4 [61], in the bud2-2 plant were on lateral root formation, in contrast to wild-type plants significantly attenuated after 60 min of IAA treatment (Figure 2A), indicating that the bud2 plant is relatively (Figure 2C). Taken together, these results indicate that insensitive to exogenous auxin in promoting lateral root auxin signaling is defective in bud2 mutant plants. formation. Furthermore, we assayed the auxin effect on the axillary bud outgrowth using a split plate procedure Induction of BUD2 by auxin reported previously [22]. As shown in Figure 2B, the To determine whether BUD2 expression is regulated exogenous NAA almost completely inhibited the axillary by auxin or cytokinin, we determined the BUD2 expres- bud outgrowth of the wild-type plants, but it showed no sion levels in wild-type seedlings on auxin and cytoki- significant impeding effect on bud2 and axr1-3, a mutant nin treatments. RNA gel blot analysis revealed that the defective in the auxin-signaling pathway [60].
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