ZmCCD7/ZpCCD7 encodes a carotenoid cleavage dioxygenase mediating shoot branching

Planta

Volumn 243, Issue 6, 2016, Pages 1407-1418

  Pan, Xiaoying ^a   Zheng, Hongyan ^a   Zhao, Jianyu ^a   Xu, Yanjun ^a   Li, Xuexian ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

Carotenoid; Carotenoid cleavage dioxygenase 7 (CCD7); Phosphorus limitation; Zea mays; Zea. ssp. parviglumis

Indexed keywords

CAROTENOID; DIOXYGENASE; LACTONE; PHOSPHORUS; PLANT PROTEIN;

BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MAIZE; METABOLISM; MOLECULAR CLONING; PHYSIOLOGY; SHOOT;

BIOSYNTHETIC PATHWAYS; CAROTENOIDS; CLONING, MOLECULAR; DIOXYGENASES; GENE EXPRESSION REGULATION, PLANT; LACTONES; PHOSPHORUS; PLANT PROTEINS; PLANT SHOOTS; ZEA MAYS;

EID: 84971664802     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-016-2479-5     Document Type: Article

References (73)

1. Abbe EC, Stein OL (1954) The growth of the shoot apex in maize: embryogeny. Am J Bot 41:285–293
2. Abe S, Sado A, Tanaka K (2014) Carlactone is converted to carlactonoic acid by MAX1 in Arabidopsis and its methyl ester can directly interact with AtD14 in vitro. P Natl Acad Sci USA 111:18084–18089
3. Aguilar-Martínez JA, Poza-Carrión C, Cubas P (2007) Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. Plant Cell 19:458–472
4. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827
5. Al-Babili S, Bouwmeester HJ (2015) Strigolactones, a novel carotenoid-derived plant hormone. Annu Rev Plant Biol 66:161–186
6. Alder A, Jamil M, Marzorati M et al (2012) The path from β-carotene to carlactone, a strigolactone-like plant hormone. Science 335:1348–1351
7. Arite T, Kameoka H, Kyozuka J (2012) Strigolactone positively controls crown root elongation in rice. J Plant Growth Regul 31:165–172
8. Auldridge ME, Block A, Vogel JT et al (2006a) Characterization of three members of the Arabidopsis carotenoid cleavage dioxygenase family demonstrates the divergent roles of this multifunctional enzyme family. Plant J 45:982–993
9. Auldridge ME, McCarty DR, Klee HJ (2006b) Plant carotenoid cleavage oxygenases and their apocarotenoids products. Curr Opin Plant Biol 9:315–321
10. Bernard P, Couturier M (1992) Cell killing by the F plasmid CcdB protein involves poisoning of DNA-topo-isomerase Π complexes. J Mol Biol 226:735–745
11. Bernard P, Kezdy K, Van Melderen L et al (1993) The F plasmid CcdB protein induces efficient ATP-dependent DNA cleavage by gyrase. J Mol Biol 234:534–541
12. Booker J, Auldridge M, Wills S et al (2004) MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule. Curr Biol 14:1232–1238
13. Bruno M, Hofmann M, Vermathen M et al (2014) On the substrate- and stereospecificity of the plant carotenoid cleavage dioxygenase 7. FEBS Lett 588:1802–1807
14. Cardoso C, Ruyter-Spira C, Bouwmeester HJ (2011) Strigolactones and root infestation by plant-parasitic Striga, Orobanche and Phelipanche spp. Plant Sci 180:414–420
15. Chatfield SP, Stimberg P, Forde BG, Leyser O (2000) The hormonal regulation of axillary bud growth in Arabidopsis. Plant J 24:159–169
16. Cline MG (1991) Apical dominance. Bot Rev 57:318–358
17. Cook CE, Whichard LP, Turner B, Wall ME, Egley GH (1966) Germination of witchweed (Striga lutea Lour.): isolation and properties of a potent stimulant. Science 154:1189–1190
18. Cook CE, Whichard LP, WallE M, Egley GH, Coggon P, Luhan PA, McPhail AT (1972) Germination stimulants. II. The structure of strigol-a potent seed germination stimulant for witchweed (Striga lutea Lour.). J Am Chem Soc 94:6198–9199
19. Cunningham FX, Gantt E (1998) Genes and enzymes of carotenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol 49:557–583
20. Czarnecki O, Yang J, Wang X, Wang S, Muchero W, Tuskan GA, Chen JG (2014) Characterization of MORE AXILLARY GROWTH genes in Populus. PLoS ONE 9:e102757
21. Desfeux C, Clough SJ, Bent AF (2000) Female reproductive tissues are the primary target of Agrobacterium-mediated transformation by the Arabidopsis floral-dip Method. Plant Physiol 123:895–904
22. Doebley J (2004) The genetics of maize evolution. Annu Rev Genet 38:37–59
23. Doebley J, Stec A, Hubbard L (1997) The evolution of apical dominance in maize. Nature 386:485–488
24. Dun EA, Brewer PB, Beveridge CA (2009) Strigolactones: discovery of the elusive shoot branching hormone. Trends Plant Sci 14:364–372
25. Earley KW, Haag JR, Pontes O, Opper K, Juehne T, Song K, Pikaard CS (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J 45:616–629
26. Evers JB, van der Krol AR, Jan Vos et al (2011) Understanding shoot branching by modelling form and function. Trends Plant Sci 16:464–467
27. Floss DS, Walter MH (2009) Role of carotenoid cleavage dioxygenase 1 (CCD1) in apocarotenoid biogenesis revisited. Plant Signal Behav 4:172–175
28. Gomez-Roldan V, Fermas S, Brewer PB et al (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194
29. Guan JC, Koch KE, Suzuki M et al (2012) Diverse roles of strigolactone signaling in maize architecture and the uncoupling of a branching-specific subnetwork. Plant Physiol 160:1303–1317
30. Hempel FD, Feldman LJ (1994) Bi-directional inflorescence development in Arabidopsis thaliana: acropetal initiation of flowers and basipetal initiation of paraclades. Planta 192:276–286
31. Hochholdinger F, Woll K, Sauer M et al (2004) Genetic dissection of root formation in maize (Zea mays) reveals root-type specific developmental programmes. Ann Bot 93:359–368
32. Jamil M, Kanampiu FK, Karaya H, Chatnikhova T, Bouwmeester HJ (2012) Striga hermonthica parasitism in maize in response to N and P fertilisers. Field Crops Res 134:1–10
33. Johnson PF, McKnight SL (1989) Eucaryotic transcriptional regulatory proteins. Annu Rev Biochem 58:799–840
34. Johnson X, Brcich T, Dun EA et al (2006) Branching genes are conserved across species: genes controlling a novel signal in pea are coregulated by other long-distance signals. Plant Physiol 142:1014–1026
35. Kapulnik Y, Delaux PM, Resnick N et al (2011) Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta 233:209–216
36. Koltai H, LekKala SP, Bhattacharya C et al (2010) A tomato strigolactone-impaired mutant displays aberrant shoot morphology and plant interactions. J Exp Bot 61:1739–1749
37. Koren D, Resnick N, Mayzlish-Gati E et al (2013) Strigolactone signaling in the endodermis is sufficient to restore root responses and involves SHORT HYPOCOTYL 2 (SHY2) activity. New Phytol 198:66–874
38. Lafever HN (1981) Genetic-differences in plant-response to soil nutrient stress. J Plant Nutr 4:89–109
39. Li XY, Qian Q, Fu ZM et al (2003) Control of tillering in rice. Nature 422:618–621
40. Liao CS, Peng YF, Ma W et al (2012) Proteomic analysis revealed nitrogen-mediated metabolic, developmental, and hormonal regulation of maize (Zea mays L.) ear growth. J Exp Bot 14:5275–5288
41. T method. Methods 25:402–408
42. Lopez-Obando M, Ligerot Y, Bonhomme S, Boyer FD, Rameau C (2015) Strigolactone biosynthesis and signaling in plant development. Development 142:3615–3619
43. Minakuchi K, Kameoka H, Yasuno N et al (2010) FINE CULM1 (FC1) works downstream of strigolactones to inhibit the outgrowth of axillary buds in rice. Plant Cell Physiol 51:1127–1135
44. Nakagawa H, Jiang CJ, Sakakibara H et al (2005) Overexpression of a petunia zinc-finger gene alters cytokinin metabolism and plant forms. Plant J 41:512–523
45. Ogden S, Haggerty D, Stoner CM, Kolodrubetz D, Schleif R (1980) The Escherichia coli L-arabinose operon: binding sites of the regulatory proteins and a mechanism of positive and negative regulation. P Natl Acad Sci USA 77:3346–3350
46. Pan XY, Hasan MM, Li YQ et al (2015) Asymmetric transcriptomic signatures between the cob and florets in the maize ear under optimal- and low-nitrogen conditions at silking, and functional characterization of amino acid transporters ZmAAP4 and ZmVAAT3. J Exp Bot. doi:10.1093/jxb/erv315
47. Ruyter-Spira C, Kohlen W, Charnikhova T et al (2011) Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another belowground role for strigolactones. Plant Physiol 155:721–734
48. Ruyter-Spira C, Al-Babili S, van der Krol S, Bouwmeester H (2013) The biology of strigolactones. Trends Plant Sci 18:72–83
49. Sang D, Chen D, Liu G et al (2014) Strigolactones regulate rice tiller angle by attenuating shoot gravitropism through inhibiting auxin biosynthesis. P Natl Acad Sci USA 111:11199–11204
50. Sangoi L, Gracietti MA, Rampazzo C et al (2002) Response of brazilian maize hybrids from different eras to changes in plant density. Field Crop Res 79:39–51
51. Sato D, Awad AA, Chse SH et al (2003) Analysis of strigolactones, germination stimulants for Striga and Orobanche, by high-performance liquid chromatography/tandem mass spectrometry. J Agric Food Chem 51:1162–1168
52. Schleif RS (1992) DNA looping. Annu Rev Biochem 61:199–223
53. Schmelz EA, Alborn HT, Tumlinson JH (2001) The influence of intact-plant and excised-leaf bioassay designs on volicitin- and jasmonic acid-induced sesquiterpene volatile release in Zea mays. Planta 214:171–179
54. Schwartz SH, Qin X, Loewen MC (2004) The biochemical characterization of two carotenoid cleavage enzymes from Arabidopsis indicates that a carotenoid-derived compound inhibits lateral branching. J Biol Chem 279:46940–46945
55. Seto Y, Yamaguchi S (2014) Strigolactone biosynthesis and perception. Curr Opin Plant Biol 21:1–6
56. Seto Y, Kameoka H, Yamaguchi S et al (2012) Recent advances in strigolactone research: chemical and biological aspects. Plant Cell Physiol 53:1843–1853
57. Seto Y, Sado A, Asami K, Hanada A, Umehara M, Akiyama K, Yamaguchi S (2014) Carlactone is an endogenous biosynthesis precursor for strigolactones. P Natl Acad Sci USA 111:1640–1645
58. Simons JL, Snowden KC (2007) Analysis of the decreased apical dominance genes of petunia in the control of axillary branching. Plant Physiol 143:697–706
59. Sun ZR, Gantt E, Jr Cunningham FX (1996) Cloning and functional analysis of the beta-carotene hydroxylase of Arabidopsis thaliana. J Biol Chem 271:24349–24352
60. Umehara M, Hanada A, Yoshida S et al (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200
61. Umehara M, Hanada A, Magome H et al (2010) Contribution of strigolactones to the inhibition of tiller bud outgrowth under phosphate deficiency in rice. Plant Cell Physiol 51:1118–1126
62. Van Ha C, Leyva-González MA, Osakabe Y et al (2014) Positive regulatory role of strigolactone in plant responses to drought and salt stress. P Natl Acad Sci USA 111:851–856
63. Vogel JT, Walter MH, Giavalisco P et al (2010) SlCCD7 controls strigolactone biosynthesis, shoot branching and mycorrhiza-induced apocarotenoid formation in tomato. Plant J 61:300–311
64. Waldie T, McCulloch H, Leyser O (2014) Strigolactones and the control of plant development: lessons from shoot branching. Plant J 79:607–622
65. Walter MH, Fester T, Strack D (2000) Arbuscular mycorrhizal fungi induce the non-mevalonate methylerythritol phosphate pathway of isoprenoid biosynthesis correlated with the accumulation of the ‘yellow pigment’ and other apocarotenoids. Plant J 21:571–578
66. Wang L, Wang B, Jiang L et al (2015) Strigolactone signaling in Arabidopsis regulates shoot development by targeting D53-like SMXL repressor proteins for ubiquitination and degradation. Plant Cell 27:3128–3142
67. Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2:1565–1572
68. Yu P, Li X, Yuan L et al (2014a) A novel morphological response of maize (Zea mays) adult roots to heterogeneous nitrate supply revealed by a split-root experiment. Physiol Plant 150:133–144
69. Yu P, White PJ, Hochholdinger F et al (2014b) Phenotypic plasticity of the maize root system in response to heterogeneous nitrogen availability. Planta 240:667–678
70. Zhang XL, Zhou Y, Ding L et al (2013) Transcription repressor HANABA TARANU controls flower development by integrating the actions of multiple hormones, floral organ specification genes, and GATA3 family genes in Arabidopsis. Plant Cell 25:83–101
71. Zhu HF, Kranz RG (2012) A nitrogen-regulated glutamine amidotransferase (GAT1_2.1) represses shoot branching in Arabidopsis. Plant Physiol 160:1770–1780
72. Zou JH, Zhang SY, Zhang WP et al (2006) The rice HIGH-TILLERING DWARF1 encoding an ortholog of Arabidopsis MAX3 is required for negative regulation of the outgrowth of axillary buds. Plant J 48:687–696
73. Zuo WL, Chao Q, Zhang N et al (2015) A maize wall-associated kinase confers quantitative resistance to head smut. Nat Genet 47:151–157