MAX3/CCD7 Is a Carotenoid Cleavage Dioxygenase Required for the Synthesis of a Novel Plant Signaling Molecule

Booker, Jonathan; Auldridge, M.E.; Wills, Sara; McCarty, Donald R.; Klee, Harry J.; Leyser, Ottoline

doi:10.1016/j.cub.2004.06.061

Cited by 506 publications

(533 citation statements)

References 31 publications

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“…Recent studies on a series of branching mutants, such as more axillary growth (max) of Arabidopsis [37][38][39][40], ramosus (rms) mutants of pea [41][42][43], decreased apical dominance (dad) mutants of petunia [44,45] and dwarf (d) mutants of rice [46][47][48][49][50][51], have revealed strigolactone as a second messenger of auxin action on the control of AM outgrowth [52,53]. Strigolactones, a group of terpenoid lactones that have been found in root exudates of diverse plant species, are synthesized from carotenoids in roots and transported acropetally or synthesized locally to repress the outgrowth of shoot branches [38,[54][55][56].…”

Section: Introductionmentioning

confidence: 99%

The BUD2 mutation affects plant architecture through altering cytokinin and auxin responses in Arabidopsis

et al. 2010

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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. IntroductionPolyamines, including diamine putrescine, triamine spermidine and tetraamine spermine, are low-molecularmass organic cations. They exist widely in all living organisms and are essential for their survival, because blocking of the biosynthesis of polyamines leads to lethal phenotypes in animals [1] and higher plants [2][3][4]. In higher plants, polyamines have been proposed to function in response to environmental stresses and in regulating growth and development [4][5][6][7][8][9][10][11]. Plant molecular and physiological studies over past decades have shown that higher plants defective in producing polyamines often have altered plant architecture, with reduced plant height or more branches in shoots and roots [4,[10][11][12][13]. However, the underlying mechanisms still remain largely elusive.Branches of higher plants originate from the axillary meristems (AMs) of shoots, and formation of a branch generally consists of the initiation of a new AM and its subsequent outgrowth. However, an AM may arrest its growth under some conditions, forming a dormant bud. The dormant buds will release their outgrowth once they sense a permissible environmental or developmental signal. In many plant species, axillary buds become dormant due to the inhibiting effects of the primary shoot apex on the outgrowth of AMs, a phenomenon known as 'apical dominance'. Auxin was first regarded as a direct regulator in this process [14], a notion strengthened thereafter by physiological studies on decapitated shoot apices [15][16][17], and by analyzing auxin biosynthesis, transport and signaling [18][19][20][21][22][23][24][25][26][27][28][29] in plants. However, when radiolabelled auxin was applied to a decapitated stump, the outgrowth of axillary buds was inhibited even though radiolabelled auxin was not found to accumulate in axillary buds, suggesting an indirect suppression effect of auxin on the AM outgrowth [28,30] and the presence of second messengers.Cytokinin has been proposed as a second messenger 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 antagonistic role of auxin and cytokinin in the regulation of apical dominance has been postu...

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Section: Introductionmentioning

confidence: 99%

The BUD2 mutation affects plant architecture through altering cytokinin and auxin responses in Arabidopsis

et al. 2010

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“…The plant hormone ABA has long been known to be involved in regulating plant responses to various environmental stresses, especially drought and salinity and also in long-distance signalling within the plant (Davies et al 2005). Furthermore, a novel, unidentiWed, apocarotenoid phytohormone that regulates plant lateral shoot branching was recently postulated to be produced from an as yet unidentiWed carotenoid substrate by sequential cleavage by CCD7 and CCD8 (Booker et al 2004;Schwartz et al 2004). In addition to being plant hormones, some of the apocarotenoids (such as -ionone, -cyclocitral, geranial, geranial acetone, theaspirone, -damascenone and -damascenone) contribute to the Xavour and/or aroma of Xowers or fruits of a variety of agricultural products (Auldridge et al 2006b).…”

Section: Introductionmentioning

confidence: 99%

Cloning and characterisation of a maize carotenoid cleavage dioxygenase (ZmCCD1) and its involvement in the biosynthesis of apocarotenoids with various roles in mutualistic and parasitic interactions

Sun¹,

Hans

Walter

et al. 2008

Planta

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Colonisation of maize roots by arbuscular mycorrhizal (AM) fungi leads to the accumulation of apocarotenoids (cyclohexenone and mycorradicin derivatives). Other root apocarotenoids (strigolactones) are involved in signalling during early steps of the AM symbiosis but also in stimulation of germination of parasitic plant seeds. Both apocarotenoid classes are predicted to originate from cleavage of a carotenoid substrate by a carotenoid cleavage dioxygenase (CCD), but the precursors and cleavage enzymes are unknown. A Zea mays CCD (ZmCCD1) was cloned by RT-PCR and characterised by expression in carotenoid accumulating E. coli strains and analysis of cleavage products using GC-MS. ZmCCD1 eYciently cleaves carotenoids at the 9, 10 position and displays 78% amino acid identity to Arabidopsis thaliana CCD1 having similar properties. ZmCCD1 transcript levels were shown to be elevated upon root colonisation by AM fungi. Mycorrhization led to a decrease in seed germination of the parasitic plant Striga hermonthica as examined in a bioassay. ZmCCD1 is proposed to be involved in cyclohexenone and mycorradicin formation in mycorrhizal maize roots but not in strigolactone formation.

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“…Likewise, RMS5, MAX3, and D17/HTD1 were found to encode CCD7 (Booker et al, 2004;Johnson et al, 2006;Zou et al, 2006). In contrast, the SMS response mutants, max2, rms4, and d3, were found to be mutated in an orthologous gene encoding an F-box protein (Stirnberg et al, 2002;Ishikawa et al, 2005;Johnson et al, 2006).…”

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confidence: 99%

Strigolactone Acts Downstream of Auxin to Regulate Bud Outgrowth in Pea and Arabidopsis

et al. 2009

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During the last century, two key hypotheses have been proposed to explain apical dominance in plants: auxin promotes the production of a second messenger that moves up into buds to repress their outgrowth, and auxin saturation in the stem inhibits auxin transport from buds, thereby inhibiting bud outgrowth. The recent discovery of strigolactone as the novel shootbranching inhibitor allowed us to test its mode of action in relation to these hypotheses. We found that exogenously applied strigolactone inhibited bud outgrowth in pea (Pisum sativum) even when auxin was depleted after decapitation. We also found that strigolactone application reduced branching in Arabidopsis (Arabidopsis thaliana) auxin response mutants, suggesting that auxin may act through strigolactones to facilitate apical dominance. Moreover, strigolactone application to tiny buds of mutant or decapitated pea plants rapidly stopped outgrowth, in contrast to applying N-1-naphthylphthalamic acid (NPA), an auxin transport inhibitor, which significantly slowed growth only after several days. Whereas strigolactone or NPA applied to growing buds reduced bud length, only NPA blocked auxin transport in the bud. Wild-type and strigolactone biosynthesis mutant pea and Arabidopsis shoots were capable of instantly transporting additional amounts of auxin in excess of endogenous levels, contrary to predictions of auxin transport models. These data suggest that strigolactone does not act primarily by affecting auxin transport from buds. Rather, the primary repressor of bud outgrowth appears to be the auxindependent production of strigolactones.

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MAX3/CCD7 Is a Carotenoid Cleavage Dioxygenase Required for the Synthesis of a Novel Plant Signaling Molecule

Abstract: We conclude that MAX3 is required for the synthesis of a novel carotenoid-derived long-range signal that regulates shoot branching.

Cited by 506 publications

References 31 publications

The BUD2 mutation affects plant architecture through altering cytokinin and auxin responses in Arabidopsis

The BUD2 mutation affects plant architecture through altering cytokinin and auxin responses in Arabidopsis

Cloning and characterisation of a maize carotenoid cleavage dioxygenase (ZmCCD1) and its involvement in the biosynthesis of apocarotenoids with various roles in mutualistic and parasitic interactions

Strigolactone Acts Downstream of Auxin to Regulate Bud Outgrowth in Pea and Arabidopsis

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