Condensed tannin biosynthesis and polymerization synergistically condition carbon use, defense, sink strength and growth in Populus

Tree Physiology

Volumn 34, Issue 11, 2014, Pages 1240-1251

  Harding, Scott A ^a,b   Xue, Liang Jiao ^a,b   Du, Lei ^a,b,e   Nyamdari, Batbayar ^a,b   Lindroth, Richard L ^c   Sykes, Robert ^d   Davis, Mark F ^d   Tsai, Chung Jui ^a,b  

^a UNIVERSITY OF GEORGIA   (United States)

^b University of Wisconsin ^*  (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d NATIONAL RENEWABLE ENERGY LABORATORY   (United States)

^e KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Flavonoid; Glycolysis; MYB; Phenylethylamine; Phenylpropanoid; Salicortin

Indexed keywords

CARBON; CHEMICAL DEFENSE; CONIFEROUS TREE; GROWTH RATE; PHENOTYPE; POLYMERIZATION; SOURCE-SINK DYNAMICS; SURVIVAL; SYNERGISM; TANNIN;

POPULUS; POPULUS FREMONTII;

1-PHENYLPROPANOL; CARBON; GLUCOSIDE; GLYCOSIDE; NITROGEN; PHENETHYLAMINE DERIVATIVE; PHENOL DERIVATIVE; PROANTHOCYANIDIN; PROPANOL; SALICORTIN;

CARBON SEQUESTRATION; CHEMISTRY; CHIMERA; DNA MICROARRAY; GENE EXPRESSION REGULATION; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; METABOLISM; METABOLOME; PLANT LEAF; POLYMERIZATION; POPULUS;

CARBON; CARBON SEQUESTRATION; CHIMERA; GENE EXPRESSION REGULATION, PLANT; GENOTYPE; GLUCOSIDES; GLYCOSIDES; METABOLOME; NITROGEN; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENETHYLAMINES; PHENOLS; PLANT LEAVES; POLYMERIZATION; POPULUS; PROANTHOCYANIDINS; PROPANOLS;

EID: 84923345253     PISSN: 0829318X     EISSN: 17584469     Source Type: Journal    
DOI: 10.1093/treephys/tpt097     Document Type: Article

References (52)

1. Ayres MP, Clausen TP, MacLean SF, Redman AM, Reichardt PB (1997) Diversity of structure and antiherbivore activity in condensed tannins. Ecology 78:1696-1712.
2. Babst BA, Harding SA, Tsai CJ (2010) Biosynthesis of phenolic glycosides from phenylpropanoid and benzenoid precursors in Populus. J Chem Ecol 36:286-297.
3. Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519-546.
4. Bryant JP, Chapin FS, Klein DR (1983) Carbon nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357-368.
5. Clausen TP, Chen J, Bryant JP, Provenza FD, Villalba J (2010) Dynamics of the volatile defense of winter 'dormant' balsam poplar (Populus balsamifera). J Chem Ecol 36:461-466.
6. Fatland BL, Nikolau BJ, Wurtele ES (2005) Reverse genetic characterization of cytosolic acetyl-CoA generation by ATP-citrate lyase in Arabidopsis. Plant Cell 17:182-203.
7. Fischer K, Kammerer B, Gutensohn M, Arbinger B, Weber A, Hausler RE, Flugge UI (1997) A new class of plastidic phosphate translocators: a putative link between primary and secondary metabolism by the phosphoenolpyruvate/phosphate antiporter. Plant Cell 9:453-462.
8. Fritz C, Palacios-Rojas N, Feil R, Stitt M (2006) Regulation of secondary metabolism by the carbon-nitrogen status in tobacco: nitrate inhibits large sectors of phenylpropanoid metabolism. Plant J 46:533-548.
9. Frost CJ, Nyamdari B, Tsai CJ, Harding SA (2012) The tonoplast-localized sucrose transporter in Populus (PtaSUT4) regulates whole-plant water relations, responses to water stress, and photosynthesis. PLoS One 7:10.
10. Harding SA, Jiang HY, Jeong ML, Casado FL, Lin HW, Tsai CJ (2005) Functional genomics analysis of foliar condensed tannin and phenolic glycoside regulation in natural cottonwood hybrids. Tree Physiol 25:1475-1486.
11. Harding SA, Jarvie MM, Lindroth RL, Tsai CJ (2009) A comparative analysis of phenylpropanoid metabolism, N utilization, and carbon partitioning in fast- and slow-growing Populus hybrid clones. J Exp Bot 60:3443-3452.
12. Haruta M, Pedersen JA, Constabel CP (2001) Polyphenol oxidase and herbivore defense in trembling aspen (Populus tremuloides): cDNA cloning, expression, and potential substrates. Physiol Plant 112:552-558.
13. Herms DA, Mattson WJ (1992) The dilemma of plants - to grow or defend. Q Rev Biol 67:283-335.
14. Holeski LM, Vogelzang A, Stanosz G, Lindroth RL (2009) Incidence of Venturia shoot blight in aspen (Populus tremuloides Michx.) varies with tree chemistry and genotype. Biochem Syst Ecol 37:139-145.
15. Holeski LM, Hillstrom ML, Whitham TG, Lindroth RL (2012) Relative importance of genetic, ontogenetic, induction, and seasonal variation in producing a multivariate defense phenotype in a foundation tree species. Oecologia 170:695-707.
16. Horbowicz M, Kosson R, Wiczkowski W, Koczkodaj D, Mitrus J (2011) The effect of methyl jasmonate on accumulation of 2-phenylethylamine and putrescine in seedlings of common buckwheat (Fagopyrum esculentum). Acta Physiol Plant 33:897-903.
17. Kandil FE, Grace MH, Seigler DS, Cheeseman JM (2004) Polyphenolics in Rhizophora mangle L. leaves and their changes during leaf development and senescence. Trees 18:518-528.
18. 2+ influx. Plant Cell Physiol 41:1259-1266.
19. Kleiner KW, Raffa KF, Dickson RE (1999) Partitioning of C-14-labeled photosynthate to allelochemicals and primary metabolites in source and sink leaves of aspen: evidence for secondary metabolite turnover. Oecologia 119:408-418.
20. Kosonen M, Keski-Saari S, Ruuhola T, Constabel CP, Julkunen-Tiitto R (2012) Effects of overproduction of condensed tannins and elevated temperature on chemical and ecological traits of genetically modified hybrid aspens (Populus tremula x P. tremuloides). J Chem Ecol 38:1235-1246.
21. Kraus TEC, Zasoski RJ, Dahlgren RA, Horwath WR, Preston CM (2004) Carbon and nitrogen dynamics in a forest soil amended with purified tannins from different plant species. Soil Biol Biochem 36: 309-321.
22. Lam HM, Coschigano KT, Oliveira IC, MeloOliveira R, Coruzzi GM (1996) The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Annu Rev Plant Physiol Plant Mol Biol 47:569-593.
23. Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9:13.
24. Levin JG, Sprinson DB (1964) The enzymatic formation and isolation of 3-enolpyruvylshikimate 5-phosphate. J Biol Chem 239:1142-1150.
25. 2 - productivity, phytochemistry, and insect performance. Ecology 74:763-777.
26. Lindroth RL, Osier TL, Barnhill HRH, Wood SA (2002) Effects of geno-type and nutrient availability on phytochemistry of trembling aspen (Populus tremuloides Michx.) during leaf senescence. Biochem Syst Ecol 30:297-307.
27. Matt P, Krapp A, Haake V, Mock HP, Stitt M (2002) Decreased Rubisco activity leads to dramatic changes of nitrate metabolism, amino acid metabolism and the levels of phenylpropanoids and nicotine in tobacco antisense RBCS transformants. Plant J 30:663-677.
28. Mellway RD, Tran LT, Prouse MB, Campbell MM, Constabel CP (2009) The wound-, pathogen-, and ultraviolet B-responsive MYB134 gene encodes an R2R3 MYB transcription factor that regulates proanthocyanidin synthesis in poplar. Plant Physiol 150:924-941.
29. Murray CL, Lumis GP, Chong C (1996) Fertilizer method and container size effects on shade trees grown in in-ground containers. Can J Plant Sci 76:507-513.
30. Mutuku JM, Nose A (2012) Changes in the contents of metabolites and enzyme activities in rice plants responding to Rhizoctonia solani Kuhn infection: activation of glycolysis and connection to phenylpropanoid pathway. Plant Cell Physiol 53:1017-1032.
31. Niehl A, Lacomme C, Erban A, Kopka J, Kramer U, Fisahn J (2006) Systemic potato virus X infection induces defence gene expression and accumulation of beta-phenylethylamine-alkaloids in potato. Funct Plant Biol 33:593-604.
32. Osier TL, Lindroth RL (2001) Effects of genotype, nutrient availability, and defoliation on aspen phytochemistry and insect performance. J Chem Ecol 27:1289-1313.
33. Payyavula RS, Babst BA, Nelsen MP, Harding SA, Tsai CJ (2009) Glycosylation-mediated phenylpropanoid partitioning in Populus tremuloides cell cultures. BMC Plant Biol 9:12.
34. Plaxton WC (1996) The organization and regulation of plant glycolysis. Annu Rev Plant Physiol Plant Mol Biol 47:185-214.
35. Porter LJ, Hrstich LN, Chan BG (1986) The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25:223-230.
36. Pourcel L, Routaboul JM, Kerhoas L, Caboche M, Lepiniec L, Debeaujon I (2005) TRANSPARENT TESTA10 encodes a laccase-like enzyme involved in oxidative polymerization of flavonoids in Arabidopsis seed coat. Plant Cell 17:2966-2980.
37. Pourcel L, Irani GN, Koo AJK, Bohorquez-Restrepo A, Howe GA, Grotewold E (2013) A chemical complementation approach reveals genes and interactions of flavonoids with other pathways. Plant J 74:1-15.
38. Ruuhola TM, Julkunen-Tiitto MRK (2000) Salicylates of intact Salix myrsinifolia plantlets do not undergo rapid metabolic turnover. Plant Physiol 122:895-905.
39. Schopfer P (1996) Hydrogen peroxide-mediated cell-wall stiffening in vitro in maize coleoptiles. Planta 199:43-49.
40. Schweitzer JA, Madritch MD, Bailey JK et al. (2008) From genes to ecosystems: the genetic basis of condensed tannins and their role in nutrient regulation in a Populus model system. Ecosystems 11:1005-1020.
41. Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant Cell Environ 30:1126-1149.
42. Smoot ME, Ono K, Ruscheinski J, Wang P-L, Ideker T (2011) Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 27:431-432.
43. Smyth GK (2005) Limma: linear models for microarray data. In: Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W (eds) Bioinformatics and computational biology solutions using R and bioconductor. Springer, New York, pp 397-420.
44. Streatfield SJ, Weber A, Kinsman EA et al. (1999) The phosphoenol pyruvate/phosphate translocator is required for phenolic metabolism, palisade cell development, and plastid-dependent nuclear gene expression. Plant Cell 11:1609-1621.
45. Tieman D, Taylor M, Schauer N, Fernie AR, Hanson AD, Klee HJ (2006) Tomato aromatic amino acid decarboxylases participate in synthesis of the flavor volatiles 2-phenylethanol and 2-phenylacetaldehyde. Proc Natl Acad Sci USA 103:8287-8292.
46. Tipton KF, Boyce S, O'Sullivan J, Davey GP, Healy J (2004) Monoamine oxidases: certainties and uncertainties. Curr Med Chem 11: 1965-1982.
47. Tsai CJ, Harding SA, Tschaplinski TJ, Lindroth RL, Yuan YN (2006) Genome-wide analysis of the structural genes regulating defense phenylpropanoid metabolism in Populus. New Phytol 172:47-62.
48. Tsai C-J, Cseke L, Harding S (2011a) Isolation and purification of RNA. In: Cseke L, Kirakosyan A, Kaufman P, Westfall M (eds) Handbook of molecular and cellular methods in biology and medicine. CRC Press, Boca Raton, NY, pp 167-186.
49. Tsai CJ, Ranjan P, DiFazio SP, Tuskan GA, Johnson V (2011b) Poplar genome microarrays. In: Joshi CP, DiFazio SP, Kole C (eds) Genetics, genomics and breeding of poplars. Science Publishers, Enfield, NH, pp 112-127.
50. Wait DA, Jones CG, Schaedle M (1996) Controlling growth and chemical composition of saplings by iteratively matching nutrient supply to demand: a bootstrap fertilization technique. Tree Physiol 16:359-365.
51. Wang HQ, Tuominen LK, Tsai CJ (2011) SLIM: a sliding linear model for estimating the proportion of true null hypotheses in datasets with dependence structures. Bioinformatics 27:225-231.
52. Wiley E, Helliker B (2012) A re-evaluation of carbon storage in trees lends greater support for carbon limitation to growth. New Phytol 195:285-289.