Investigation of triterpene synthesis and regulation in oats reveals a role for β-amyrin in determining root epidermal cell patterning

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 23, 2014, Pages 8679-8684

  Kemen, Ariane C ^a,d   Honkanen, Suvi ^a,b,e   Melton, Rachel E ^a   Findlay, Kim C ^a   Mugford, Sam T ^a   Hayashi, Keiko ^a,f   Haralampidis, Kosmas ^c   Rosser, Susan J ^b,g   Osbourn, Anne ^a  

^a JOHN INNES CENTRE   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c UNIVERSITY OF ATHENS   (Greece)

^d MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^e UNIVERSITY OF OXFORD   (United Kingdom)

^f NATIONAL AGRICULTURAL RESEARCH CENTER   (Japan)

^g UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Cell specification; Hormones; Root development

Indexed keywords

BETA AMYRIN; HOMEODOMAIN PROTEIN; LEUCINE ZIPPER PROTEIN; PHYTOSTEROL; PLANT GLYCOSIDE; SAPONIN; TRITERPENE;

AMINO ACID SEQUENCE; ARTICLE; AVENA STRIGOSA; BIOACCUMULATION; CELL FATE; CLADISTICS; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; GENE ACTIVITY; GENE DELETION; GENE DUPLICATION; GENETIC CONSERVATION; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; OAT; PHENOTYPE; PHYLOGENETIC TREE; PLANT EPIDERMIS CELL; PLANT GENE; PLANT GROWTH; PLANT METABOLISM; PLANT ROOT; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN MOTIF; ROOT DEVELOPMENT; ROOT HAIR; SAD1 GENE; SAD2 GENE; SOIL; SPECIES DIVERSITY; SYNTHESIS; WILD TYPE;

CELL SPECIFICATION; HORMONES; ROOT DEVELOPMENT;

AVENA SATIVA; CYTOCHROME P-450 ENZYME SYSTEM; GENE EXPRESSION REGULATION, PLANT; GLUCURONIDASE; GREEN FLUORESCENT PROTEINS; INTRAMOLECULAR TRANSFERASES; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; MUTATION; OLEANOLIC ACID; PHYLOGENY; PLANT EPIDERMIS; PLANT PROTEINS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SAPONINS; TRANSCRIPTOME; TRITERPENES;

EID: 84902152628     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1401553111     Document Type: Article

References (42)

1. Chappell J (2002) The genetics and molecular genetics of terpene and sterol origami. Curr Opin Plant Biol 5(2):151-157.
2. Augustin JM, Kuzina V, Andersen SB, Bak S (2011) Molecular activities, biosynthesis and evolution of triterpenoid saponins. Phytochemistry 72(6):435-457.
3. Moses T, Pollier J, Thevelein JM, Goossens A (2013) Bioengineering of plant (tri)terpenoids: From metabolic engineering of plants to synthetic biology in vivo and in vitro. New Phytol 200(1):27-43, 10.1111/nph.12325.
4. Sawai S, Saito K (2011) Triterpenoid biosynthesis and engineering in plants. Front Plant Sci 2:25.
5. Thimmappa R, Geyser K, Louveau T, O'Maille P, Osbourn A (2014) Triterpene biosynthesis in plants. Ann Rev Plant Biol 65:16.1-16.33.
6. Turner EM (1960) The nature of resistance of oats to the take-all fungus. III. Distribution of the inhibitor in oat seedlings. J Exp Bot 11:403-412.
7. Papadopoulou K, Melton RE, LeggettM, DanielsMJ, Osbourn AE (1999) Compromised disease resistance in saponin-deficient plants. Proc Natl Acad Sci USA 96(22):12923-12928. (Pubitemid 29513604)
8. Haralampidis K, et al. (2001) A new class of oxidosqualene cyclases directs synthesis of antimicrobial phytoprotectants in monocots. Proc Natl Acad Sci USA 98(23):13431-13436. (Pubitemid 33051380)
9. Qi X, et al. (2006) A different function for a member of an ancient and highly conserved cytochrome P450 family: From essential sterols to plant defense. Proc Natl Acad Sci USA 103(49):18848-18853. (Pubitemid 44913498)
10. Geisler K, et al. (2013) Biochemical analysis of a multifunctional cytochrome P450 (CYP51) enzyme required for synthesis of antimicrobial triterpenes in plants. Proc Natl Acad Sci USA 110(35):E3360-E3367.
11. Mugford ST, et al. (2009) A serine carboxypeptidase-like acyltransferase is required for synthesis of antimicrobial compounds and disease resistance in oats. Plant Cell 21(8):2473-2484.
12. Mugford ST, et al. (2013) Modularity of plant metabolic gene clusters: A trio of linked genes that are collectively required for acylation of triterpenes in oat. Plant Cell 25(3):1078-1092.
13. Owatworakit A, et al. (2013) Glycosyltransferases from oat (Avena) implicated in the acylation of avenacins. J Biol Chem 288(6):3696-3704.
14. Mylona P, et al. (2008) Sad3 and sad4 are required for saponin biosynthesis and root development in oat. Plant Cell 20(1):201-212. (Pubitemid 352844043)
15. Qi X, et al. (2004) A gene cluster for secondary metabolism in oat: Implications for the evolution of metabolic diversity in plants. Proc Natl Acad Sci USA 101(21):8233-8238. (Pubitemid 38698083)
16. Wegel E, Koumproglou R, Shaw P, Osbourn A (2009) Cell type-specific chromatin decondensation of a metabolic gene cluster in oats. Plant Cell 21(12):3926-3936.
17. Schrick K, Nguyen D, Karlowski WM, Mayer KF (2004) START lipid/sterol-binding domains are amplified in plants and are predominantly associated with homeodomain transcription factors. Genome Biol 5(6):R41.
18. Masucci JD, et al. (1996) The homeobox gene GLABRA2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana. Development 122(4):1253-1260. (Pubitemid 26123900)
19. Dolan L, et al. (1993) Cellular organisation of the Arabidopsis thaliana root. Development 119(1):71-84. (Pubitemid 23279128)
20. Datta S, et al. (2011) Root hairs: Development, growth and evolution at the plant-soil interface. Plant Soil 346:1-14.
21. Grebe M (2012) The patterning of epidermal hairs in Arabidopsis - updated. Curr Opin Plant Biol 15(1):31-37.
22. Osbourn A, et al. (1994) An oat species lacking avenacin is susceptible to infection by Gaeumannomyces graminis var. tritici. Physiol Mol Plant Pathol 45(6):457-467.
23. Abe M, Takahashi T, Komeda Y (2001) Identification of a cis-regulatory element for L1 layer-specific gene expression, which is targeted by an L1-specific homeodomain protein. Plant J 26(5):487-494. (Pubitemid 32665048)
24. Nakamura M, et al. (2006) Characterization of the class IV homeodomain-Leucine Zipper gene family in Arabidopsis. Plant Physiol 141(4):1363-1375. (Pubitemid 44223288)
25. Christensen SK, Dagenais N, Chory J, Weigel D (2000) Regulation of auxin response by the protein kinase PINOID. Cell 100(4):469-478.
26. Smith RS, et al. (2006) A plausible model of phyllotaxis. Proc Natl Acad Sci USA 103(5):1301-1306. (Pubitemid 43191160)
27. Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M (2001) Auxin regulates SCF(TIR1)-dependent degradation of AUX/IAA proteins. Nature 414(6861):271-276. (Pubitemid 33097797)
28. Hardtke CS, Berleth T (1998) The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J 17(5):1405-1411. (Pubitemid 28105519)
29. Hu R, et al. (2012) Genome-wide identification, evolutionary expansion, and expression profile of homeodomain-leucine zipper gene family in poplar (Populus trichocarpa). PLoS ONE 7(2):e31149, 10.1371/journal.pone.0031149.
30. Depège-Fargeix N, et al. (2011) Functional characterization of the HD-ZIP IV transcription factor OCL1 from maize. J Exp Bot 62(1):293-305.
31. Zou L-P, et al. (2011) Leaf rolling controlled by the homeodomain leucine zipper class IV gene Roc5 in rice. Plant Physiol 156(3):1589-1602.
32. Kubo H, Peeters AJ, Aarts MG, Pereira A, Koornneef M (1999) ANTHOCYANINLESS2, a homeobox gene affecting anthocyanin distribution and root development in Arabidopsis. Plant Cell 11(7):1217-1226.
33. Di Cristina M, et al. (1996) The Arabidopsis Athb-10 (GLABRA2) is an HD-Zip protein required for regulation of root hair development. Plant J 10(3):393-402. (Pubitemid 27108393)
34. McCallum CM, Comai L, Greene EA, Henikoff S (2000) Targeting induced local lesions IN genomes (TILLING) for plant functional genomics. Plant Physiol 123(2):439-442. (Pubitemid 30411129)
35. Qin B, et al. (2010) High throughput screening of mutants of oat that are defective in triterpene synthesis. Phytochemistry 71(11-12):1245-1252.
36. Delis C, et al. (2011) Role of lupeol synthase in Lotus japonicus nodule formation. New Phytol 189(1):335-346.
37. Field B, Osbourn AE (2008) Metabolic diversification - independent assembly of operon-like gene clusters in different plants. Science 320(5875):543-547. (Pubitemid 351590669)
38. Thomas CL, Schmidt D, Bayer EM, Dreos R, Maule AJ (2009) Arabidopsis plant homeodomain finger proteins operate downstream of auxin accumulation in specifying the vasculature and primary root meristem. Plant J 59(3):426-436.
39. Karimi M, Inzé D, Depicker A (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7(5):193-195. (Pubitemid 36725938)
40. Amoah BK, Wu H, Sparks C, Jones HD (2001) Factors influencing Agrobacterium-mediated transient expression of uidA in wheat inflorescence tissue. J Exp Bot 52(358):1135-1142. (Pubitemid 32623705)
41. Horst I, et al. (2007) TILLING mutants of Lotus japonicus reveal that nitrogen assimilation and fixation can occur in the absence of nodule-enhanced sucrose synthase. Plant Physiol 144(2):806-820. (Pubitemid 46944745)
42. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4):402-408. (Pubitemid 34164012)