Evolution of root-specific carotenoid precursor pathways for apocarotenoid signal biogenesis

Plant Science

Volumn 233, Issue , 2015, Pages 1-10

  Walter, Michael H ^a   Stauder, Ron ^a   Tissier, Alain ^a  

^a LEIBNIZ INSTITUTE OF PLANT BIOCHEMISTRY   (Germany)

Author keywords

1 Deoxy d xylulose 5 phosphate synthase (DXS); Apocarotenoids; Arbuscular mycorrhiza; Mycorradicin; Phytoene synthase (PSY); Strigolactones

Indexed keywords

DICOTYLEDONEAE; FUNGI; LILIOPSIDA;

CAROTENOID;

ADAPTATION; EVOLUTION; METABOLISM; PHYSIOLOGICAL STRESS; PLANT PHYSIOLOGY; PLANT ROOT;

ADAPTATION, BIOLOGICAL; BIOLOGICAL EVOLUTION; CAROTENOIDS; PLANT PHYSIOLOGICAL PHENOMENA; PLANT ROOTS; STRESS, PHYSIOLOGICAL;

EID: 84921026023     PISSN: 01689452     EISSN: 18732259     Source Type: Journal    
DOI: 10.1016/j.plantsci.2014.12.017     Document Type: Review

References (83)

1. Walter M.H., Strack D. Carotenoids and their cleavage products: biosynthesis and functions. Nat. Prod. Rep. 2011, 28:663-692.
2. Sauter A., Davies W.J., Hartung W. The long-distance abscisic acid signal in the droughted plant: the fate of the hormone on its way from root to shoot. J. Exp. Bot. 2001, 52:1991-1997.
3. Farre G., et al. Travel advice on the road to carotenoids in plants. Plant Sci. 2010, 179:28-48.
4. Eroglu A., Harrison E.H. Carotenoid metabolism in mammals, including man: formation, occurrence, and function of apocarotenoids. J. Lipid Res. 2013, 54:1719-1730.
5. Sui X.W., Kiser P.D., von Lintig J., Palczewski K. Structural basis of carotenoid cleavage: from bacteria to mammals. Arch. Biochem. Biophys. 2013, 539:203-213.
6. Kloer D.P., Ruch S., Al-Babili S., Beyer P., Schulz G.E. The structure of a retinal-forming carotenoid oxygenase. Science 2005, 308:267-269.
7. Nambara E., Marion-Poll A. Abscisic acid biosynthesis and catabolism. Annu. Rev. Plant Biol. 2005, 56:165-185.
8. Boursiac Y., et al. ABA transport and transporters. Trends Plant Sci. 2013, 18:325-333.
9. Dodd I.C. Root-to-shoot signalling: assessing the roles of 'up' in the up and down world of long-distance signalling in planta. Plant Soil 2005, 274:251-270.
10. Kohlen W., et al. Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in nonarbuscular mycorrhizal host Arabidopsis. Plant Physiol. 2011, 155:974-987.
11. Maier W., Peipp H., Schmidt J., Wray V., Strack D. Levels of a terpenoid glycoside (Blumenin) and cell wall-bound phenolics in some cereal mycorrhizas. Plant Physiol. 1995, 109:465-470.
12. Klingner A., Bothe H., Wray V., Marner F.J. Identification of a yellow pigment formed in maize roots upon mycorrhizal colonization. Phytochemistry 1995, 38:53-55.
13. Fester T., et al. Occurrence and localization of apocarotenoids in arbuscular mycorrhizal plant roots. Plant Cell Physiol. 2002, 43:256-265.
14. Walter M.H. Role of carotenoid metabolism in the arbuscular mycorrhizal symbiosis. Molecular Microbial Ecology of the Rhizosphere 2013, 513-524. Wiley-Blackwell. F. de Bruijn (Ed.).
15. Recorbet G., Abdallah C., Renaut J., Wipf D., Dumas-Gaudot E. Protein actors sustaining arbuscular mycorrhizal symbiosis: underground artists break the silence. New Phytol. 2013, 199:26-40.
16. Walter M.H., Floss D.S., Strack D. Apocarotenoids: hormones, mycorrhizal metabolites and aroma volatiles. Planta 2010, 232:1-17.
17. Bucher M., Hause B., Krajinski F., Küster H. Through the doors of perception to function in arbuscular mycorrhizal symbioses. New Phytol. 2014, 204:833-840.
18. Matusova R., et al. The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiol. 2005, 139:920-934.
19. Akiyama K., Matsuzaki K., Hayashi H. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 2005, 435:824-827.
20. Lopez-Raez J.A., et al. Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytol. 2008, 178:863-874.
21. Vogel J.T., et al. SlCCD7 controls strigolactone biosynthesis, shoot branching and mycorrhiza-induced apocarotenoid formation in tomato. Plant J. 2010, 61:300-311.
22. Kohlen W., et al. The tomato CAROTENOID CLEAVAGE DIOXYGENASE8 (SlCCD8) regulates rhizosphere signaling, plant architecture and affects reproductive development through strigolactone biosynthesis. New Phytol. 2012, 196:535-547.
23. Gomez-Roldan V., et al. Strigolactone inhibition of shoot branching. Nature 2008, 455:189-194.
24. Umehara M., et al. Inhibition of shoot branching by new terpenoid plant hormones. Nature 2008, 455:195-200.
25. Koltai H. Strigolactones are regulators of root development. New Phytol. 2011, 190:545-549.
26. Kapulnik Y., Koltai H. Strigolactone involvement in root development, response to abiotic stress and interactions with the biotic soil environment. Plant Physiol. 2014, 166:560-569.
27. Koltai H. Implications of non-specific strigolactone signaling in the rhizosphere. Plant Sci. 2014, 225:9-14.
28. Proust H., et al. Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens. Development 2011, 138:1531-1539.
29. Delaux P.M., et al. Origin of strigolactones in the green lineage. New Phytol. 2012, 195:857-871.
30. Cardoso C., Ruyter-Spira C., Bouwmeester H.J. Strigolactones and root infestation by plant-parasitic Striga, Orobanche and Phelipanche spp. Plant Sci. 2011, 180:414-420.
31. Akiyama K., Ogasawara S., Ito S., Hayashi H. Structural requirements of strigolactones for hyphal branching in AM fungi. Plant Cell Physiol. 2010, 51:1104-1117.
32. Waldie T., McCulloch H., Leyser O. Strigolactones and the control of plant development: lessons from shoot branching. Plant J. 2014, 79:607-622.
33. Sun H., et al. Strigolactones are involved in phosphate- and nitrate-deficiency-induced root development and auxin transport in rice. J. Exp. Bot. 2014, 65:6735-6746.
34. Kretzschmar T., et al. A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 2012, 483:341-344.
35. Bennett T., Leyser O. Strigolactone signalling: standing on the shoulders of dwarfs. Curr. Opin. Plant Biol. 2014, 22:7-13.
36. Hamiaux C., et al. DAD2 is an alpha/beta hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr. Biol. 2012, 22:2032-2036.
37. Lopez-Raez J.A., Pozo M.J., Garcia-Garrido J.M. Strigolactones: a cry for help in the rhizosphere. Botany 2011, 89:513-522.
38. Foo E., Davies N.W. Strigolactones promote nodulation in pea. Planta 2011, 234:1073-1081.
39. Yoneyama K., et al. Strigolactones, host recognition signals for root parasitic plants and arbuscular mycorrhizal fungi, from Fabaceae plants. New Phytol. 2008, 179:484-494.
40. Van Norman J., et al. Periodic root branching in Arabidopsis requires synthesis of an uncharacterized carotenoid derivative. Proc. Natl. Acad. Sci. U. S. A. 2014, E1300-E1309.
41. Sieburth L.E., Lee D.K. BYPASS1: how a tiny mutant tells a big story about root-to-shoot signaling. J. Integr. Plant Biol. 2010, 52:77-85.
42. Avendano-Vazquez A.O., et al. An uncharacterized apocarotenoid-derived signal generated in zeta-carotene desaturase mutants regulates leaf development and the expression of chloroplast and nuclear genes in Arabidopsis. Plant Cell 2014, 26:2524-2537.
43. Frusciante S., et al. Novel carotenoid cleavage dioxygenase catalyzes the first dedicated step in saffron crocin biosynthesis. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:12246-12251.
44. Alder A., et al. The path from beta-carotene to carlactone, a strigolactone-like plant hormone. Science 2012, 335:1348-1351.
45. Lin H., et al. DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 2009, 21:1512-1525.
46. Abe S., et al. Carlactone is converted to carlactonoic acid by MAX1 in Arabidopsis and its methyl ester can directly interact with AtD14 in vitro. Proc. Natl. Acad. Sci. U. S. A. 2014, 11:18084-18089.
47. Zhang Y., et al. Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis. Nat. Chem. Biol. 2014, 10:1028-1033.
48. Bruno M., et al. On the substrate- and stereospecificity of the plant carotenoid cleavage dioxygenase 7. Febs Lett. 2014, 588:1802-1807.
49. Floss D.S., Schliemann W., Schmidt J., Strack D., Walter M.H. RNA interference-mediated repression of MtCCD1 in mycorrhizal roots of Medicago truncatula causes accumulation of C-27 apocarotenoids, shedding light on the functional role of CCD1. Plant Physiol. 2008, 148:1267-1282.
50. Jorgensen K., et al. Metabolon formation and metabolic channeling in the biosynthesis of plant natural products. Curr. Opin. Plant Biol. 2005, 8:280-291.
51. Ruiz-Sola M.A., Rodriguez-Concepcion M. Carotenoid biosynthesis in Arabidopsis: a colorful pathway. Arabidopsis Book 2012, 10:e0158.
52. Fraser P.D., Schuch W., Bramley P.M. Phytoene synthase from tomato (Lycopersicon esculentum) chloroplasts - partial purification and biochemical properties. Planta 2000, 211:361-369.
53. Parry A.D., Horgan R. Carotenoids and abscisic-acid (ABA) biosynthesis in higher plants. Physiol. Plant. 1991, 82:320-326.
54. Neill S.J., Horgan R., Parry A.D. The carotenoid and abscisic-acid content of viviparous kernels and seedlings of Zea mays L. Planta 1986, 169:87-96.
55. Li F.Q., Vallabhaneni R., Wurtzel E.T. PSY3, a new member of the phytoene synthase gene family conserved in the Poaceae and regulator of abiotic stress-induced root carotenogenesis. Plant Physiol. 2008, 146:1333-1345.
56. Welsch R., Wust F., Bar C., Al-Babili S., Beyer P. A third phytoene synthase is devoted to abiotic stress-induced abscisic acid formation in rice and defines functional diversification of phytoene synthase genes. Plant Physiol. 2008, 147:367-380.
57. Ruiz-Sola M.A., Arbona V., Gomez-Cadenas A., Rodriguez-Concepcion M., Rodriguez-Villalon A. A root specific induction of carotenoid biosynthesis contributes to ABA production upon salt stress in Arabidopsis. PLoS ONE 2014, 9:e90765.
58. Lopez-Raez J.A., et al. Differential spatio-temporal expression of carotenoid cleavage dioxygenases regulates apocarotenoid fluxes during AM symbiosis. Plant Sci. 2015, 230:59-69.
59. Favre P., et al. A novel bioinformatics pipeline to discover genes related to arbuscular mycorrhizal symbiosis based on their evolutionary conservation pattern among higher plants. BMC Plant Biol. 2014, 14:333.
60. Fantini E., Falcone G., Frusciante S., Giliberto L., Giuliano G. Dissection of tomato lycopene biosynthesis through virus-induced gene silencing. Plant Physiol. 2013, 163:986-998.
61. Walter M.H., Fester T., Strack D. Arbuscular mycorrhizal fungi induce the non-mevalonate methylerythritol phosphate pathway of isoprenoid biosynthesis correlated with accumulation of the 'yellow pigment' and other apocarotenoids. Plant J. 2000, 21:571-578.
62. Walter M.H., Hans J., Strack D. Two distantly related genes encoding 1-deoxy-d-xylulose 5-phosphate synthases: differential regulation in shoots and apocarotenoid-accumulating mycorrhizal roots. Plant J. 2002, 31:243-254.
63. Floss D.S., et al. Knock-down of the MEP pathway isogene 1-deoxy-d-xylulose 5-phosphate synthase 2 inhibits formation of arbuscular mycorrhiza-induced apocarotenoids, and abolishes normal expression of mycorrhiza-specific plant marker genes. Plant J. 2008, 56:86-100.
64. Hans J., Hause B., Strack D., Walter M.H. Cloning, characterization, and immunolocalization of a mycorrhiza-inducible 1-deoxy-d-xylulose 5-phosphate reductoisomerase in arbuscule-containing cells of maize. Plant Physiol. 2004, 134:614-624.
65. Fester T., et al. Stimulation of carotenoid metabolism in arbuscular mycorrhizal roots. Planta 2002, 216:148-154.
66. Paetzold H., et al. The isogene 1-deoxy-d-xylulose 5-phosphate synthase 2 controls isoprenoid profiles, precursor pathway allocation, and density of tomato trichomes. Mol. Plant 2010, 3:904-916.
67. Saladie M., et al. The 2-C-methylerythritol 4-phosphate pathway in melon is regulated by specialized isoforms for the first and last steps. J. Exp. Bot. 2014, 65:5077-5092.
68. Walter M.H., et al. Control of plastidial precursor supply: divergent 1-deoxy-d-xylulose 5-phosphate synthase (DXS) isogenes regulate the allocation to primary or secondary metabolism. Isoprenoid Synthesis in Plants and Microorganisms 2013, 251-270. Springer, New York. T.J. Bach, M. Rohmer (Eds.).
69. Phillips M.A., et al. Functional identification and differential expression of 1-deoxy-d-xylulose 5-phosphate synthase in induced terpenoid resin formation of Norway spruce (Picea abies). Plant Mol. Biol. 2007, 65:243-257.
70. Willmann M., et al. Mycorrhizal phosphate uptake pathway in maize: vital for growth and cob development on nutrient poor agricultural and greenhouse soils. Front. Plant Sci. 2013, 4. 10.3389/fpls.2013.00533.
71. Bartley G.E., Viitanen P.V., Bacot K.O., Scolnik P.A. A tomato gene expressed during fruit ripening encodes an enzyme of the carotenoid biosynthesis pathway. J. Biol. Chem. 1992, 267:5036-5039.
72. Bartley G.E., Scolnik P.A. cDNA cloning, expression during development, and genome mapping of Psy2, a 2nd tomato gene encoding phytoene synthase. J. Biol. Chem. 1993, 268:25718-25721.
73. Giorio G., Stigliani A.L., D'Ambrosio C. Phytoene synthase genes in tomato (Solanum lycopersicum L.) - new data on the structures, the deduced amino acid sequences and the expression patterns. FEBS J. 2008, 275:527-535.
74. Sato S., et al. The tomato genome sequence provides insights into fleshy fruit evolution. Nature 2012, 485:635-641.
75. Li F.Q., Vallabhaneni R., Yu J., Rocheford T., Wurtzel E.T. The maize phytoene synthase gene family: overlapping roles for carotenogenesis in endosperm, photomorphogenesis, and thermal stress tolerance. Plant Physiol. 2008, 147:1334-1346.
76. Arango J., Wust F., Beyer P., Welsch R. Characterization of phytoene synthases from cassava and their involvement in abiotic stress-mediated responses. Planta 2010, 232:1251-1262.
77. Peng G., et al. The role of 1-deoxy-d-xylulose-5-phosphate synthase and phytoene synthase gene family in citrus carotenoid accumulation. Plant Physiol. Biochem. 2013, 71:67-76.
78. Fu X., et al. Involvement of multiple phytoene synthase genes in tissue and cultivar-specific accumulation of carotenoids in loquat. J. Exp. Bot. 2014, 16:4679-4689.
79. Buckner B., Miguel P.S., Janick-Buckner D., Bennetzen J.L. The y1 gene of maize codes for phytoene synthase. Genetics 1996, 143:479-488.
80. Bowman M.J., Willis D.K., Simon P.W. Transcript abundance of phytoene synthase 1 and phytoene synthase 2 is associated with natural variation of storage root carotenoid pigmentation. J. Am. Soc. Horticult. Sci. 2014, 139:63-68.
81. Lopez-Raez J.A., Charnikhova T., Fernandez I., Bouwmeester H., Pozo M.J. Arbuscular mycorrhizal symbiosis decreases strigolactone production in tomato. J. Plant Physiol. 2011, 168:294-297.
82. Besserer A., et al. Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol. 2006, 4:1239-1247.
83. 2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytol. 2013, 198:190-202.