IAA–amido synthetase activity and GH3 expression during development of pea seedlings

• Autorzy: Ostrowski M. , Swidzinski M. , Ciarkowska A. , Jakubowska A.
• Języki publikacji: EN

Abstrakty

EN

Indole-3-acetic acid (IAA) conjugation is an integral component of a sensitive mechanism for the regulation of free auxin level in the cell, in addition to hormone synthesis, degradation and transport. One mechanism of regulating both the level and biological activity of hormone involves the conjugation of IAA to amino acids through IAA–amido synthetases. These enzymes belong to the family of GH3 proteins encoded by early-auxin responsive genes, which are conserved in monocots and dicots. In this investigation, we identified pea IAA–Asp synthetase as a member of the GH3 family proteins based on amino acid sequence determined by tandem mass spectrometry (LC–MS/MS). IAA–Asp synthetase was highly homologous (54–84 % amino acid identity) to the GH3 proteins from Populus trichocarpa, Glycine max, Riccinus communis, Nicotiana tabacum, and Arabidopsis thaliana. Moreover, we studied the subcellular distribution and activity of IAA amido synthetase in developing pea seedlings. The cytoplasmic localization of GH3 IAA amido synthetase was indicated in 12-day-old pea seedlings by immunofluorescence method using anti-AtGH3.5 antibodies. This finding was confirmed by the measurement of the enzyme activity in the subcellular fractions collected by differential centrifugation. The most of IAA–Asp synthetase activity (88 % of the total activity) was detected in the 100,000×g supernatant fluid fraction containing soluble cytoplasmic proteins. 3- and 6-day-old pea seedlings showed a weak IAA–Asp synthetase activity and GH3 mRNA level. Twelve-day-old pea stems exhibited 19-fold, and 4-fold higher levels of transcript and the enzyme activity, respectively than 3-day-old plants. We hypothesized that IAA–amido synthetase expression and activity depend on developmental stage of vegetative tissues and this is associated with changes in free IAA level.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2014
• Tom: 36
• Numer: 11
• Opis fizyczny: p.3029-3037,fig.,ref.

Twórcy

autor

Ostrowski M.

• Department of Biochemistry, Nicolaus Copernicus University, Gagarina 9, 87-100, Torun, Poland

autor

Swidzinski M.

• Department of Cell Biology, Nicolaus Copernicus University, Lwowska 1, 87-100, Torun, Poland

autor

Ciarkowska A.

• Department of Biochemistry, Nicolaus Copernicus University, Gagarina 9, 87-100, Torun, Poland

autor

Jakubowska A.

• Department of Biochemistry, Nicolaus Copernicus University, Gagarina 9, 87-100, Torun, Poland

Bibliografia

• Barbez E, Kleine-Vehn J (2013) Divide Et Impera—cellular auxin compartmentalization. Curr Opin Plant Biol 16:78–84
• Bierfreund NM, Tintelnot S, Reski R, Decker EL (2004) Loss of GH3 function does not affect phytochrome-mediated development in a moss, Physcomitrella patens. J Plant Physiol 161:823–835
• Böttcher C, Keyzers RA, Boss PK, Davies C (2010) Sequestration of auxin by the indole-3-acetic acid-amido synthetase GH3-1 in grape berry (Vitis vinifera L.) and the proposed role of auxin conjugation during ripening. J Exp Bot 61:3615–3625
• Böttcher C, Boss PK, Davies C (2011) Acyl substrate preferences of an IAA–amido synthetase account for variations in grape (Vitis vinifera L.) berry ripening caused by different auxinic compounds indicating the importance of auxin conjugation in plant development. J Exp Bot 62:4267–4280
• Böttcher C, Burbidge CA, Boss PK, Davies C (2013) Interactions between ethylene and auxin are crucial to the control of grape (Vitis vinifera L.) berry ripening. BMC Plant Biol 13:222–235
• Bradford MM (1976) A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
• Campanella JJ, Olajide AF, Magnus V, Ludwig-Müller J (2004) A novel auxin conjugate hydrolase from wheat with substrate specificity for longer side-chain auxin amide conjugates. Plant Physiol 135:2230–2240
• Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, Miersch O, Wasternack C, Solano R (2009) (+)-7-iso-Jasmonyl-L-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol 5:344–350
• Fu J, Liu H, Li Y, Yu H, Li X, Xiao J, Wang S (2011a) Manipulating broad-spectrum disease resistance by suppressing pathogen-induced auxin accumulation in rice. Plant Physiol 155:589–602
• Fu J, Yu H, Li X, Xiao J, Wang S (2011b) Rice GH3 gene family: regulators of growth and development. Plant Signal Behav 6:570–574
• González-Lamothe R, El Oirdi M, Brisson N, Bouarab K (2012) The conjugated auxin indole-3-acetic acid-aspartic acid promotes plant disease development. Plant Cell 24:762–777
• Gutierrez L, Mongelard G, Floková K, Păcurar DI, Novák O, Staswick P, Kowalczyk M, Păcurar M, Demailly H, Geiss G, Bellini C (2012) Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis. Plant Cell 24:2515–2527
• Hagen G, Martin G, Li Y, Guilfoyle TJ (1991) Auxin-induced expression of the soybean GH3 promoter in transgenic tobacco plants. Plant Mol Biol 17:567–579
• Hayashi K, Tan X, Zheng N, Hatate T, Kimura Y, Kepinski S, Nozaki H (2008) Small-molecule agonists and antagonists of F-box protein-substrate interactions in auxin perception and signalling. Proc Natl Acad Sci USA 105:5632–5637
• Hsieh H-L, Okamoto H, Wang M, Ang L-H, Matsui M, Goodman H, Deng XW (2000) FIN219, an auxin-regulated gene, defines a link between phytochrome A and the downstream regulator COP1 in light control of Arabidopsis development. Genes Dev 14:1958–1970
• Katsir L, Schilmiller AL, Staswick PE, He SY, Howe GA (2008) COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci USA 105:7100–7105
• Korasick DA, Enders TA, Strader LC (2013) Auxin biosynthesis and storage forms. J Exp Bot 64:2541–2555
• Kumar R, Agarwal P, Tyagi AK, Sharma AK (2012) Genome-wide investigation and expression analysis suggest diverse roles of auxin-responsive GH3 genes during development and response to different stimuli in tomato (Solanum lycopersicum). Mol Genet Genomics 287:221–235
• LeClere S, Tallez R, Rampey RA, Matsuda SPT, Bartel B (2002) Characterization of a family of IAA–amino acid conjugate hydrolases from Arabidopsis. J Biol Chem 277:20446–20452
• Liu K, Kang B-C, Jiang H, Moore SL, Li H, Watkins CB, Setter TL, Jahn MM (2005) A GH3-like gene, CcGH3, isolated from Capsicum chinense L. fruit is regulated by auxin and ethylene. Plant Mol Biol 58:447–464
• Liu K, Lee H-J, Leong SS, Liu C-L, Chou J-C (2007) A bacterial indole-3-acetyl-L-aspartic acid hydrolase inhibits mung bean (Vigna radiata L.) seed germination through arginine-rich intracellular delivery. J Plant Growth Regul 26:278–284
• Loake G, Grant M (2007) Salicylic acid in plant defence—the players and protagonists. Curr Opin Plant Biol 10:466–472
• Ludwig-Müller J (2011) Auxin conjugates: their role for plant development and in the evolution of land plants. J Exp Bot 62:1757–1773
• Ludwig-Müller J, Jülke S, Bierfreund NM, Decker EL, Reski R (2008) Moss (Physcomitrella patens) GH3 proteins act in auxin homeostasis. New Phytol 181:323–338
• Mravec J, Skůpa P, Bailly A, Hoyerová K, Křeček P, Bielach A, Petrášek J, Zhang J, Gaykova V, Stierhof Y-D, Dobrev PI, Schwarzerová K, Rolčik J, Seifertová D, Luschnig C, Benková E, Zažimalová E, Geisler M, Friml J (2009) Subcellular homeostasis of phytohormone auxin is mediated by the ERlocalized PIN5 transporter. Nature 459:1136–1140
• Oetiker JH, Aeschbacher G (1997) Temperature-sensitive plant cells with shunted indole-3-acetic acid conjugation. Plant Physiol 114:1385–1395
• Okrent RA, Wildermuth MC (2011) Evolutionary history of the GH3 family of acyl adenylases in rosids. Plant Mol Biol 76:489–505
• Ostrowski M, Jakubowska A (2008) Identification of enzyme activity that conjugates indole-3-acetic acid to aspartate in immature seeds of pea (Pisum sativum). J Plant Physiol 165:564–569
• Ostrowski M, Jakubowska A (2011) Purification and biochemical characterization of indole-3-acetyl-aspartic acid synthetase from immature seeds of pea (Pisum sativum). J Plant Growth Regul 30:30–40
• Ostrowski M, Jakubowska A (2013) GH3 expression and IAA–amide synthetase activity in pea (Pisum sativum L.) seedlings are regulated by light, plant hormones and auxinic herbicides. J Plant Physiol 170:361–368
• Peer WA (2013) From perception to attenuation: auxin signalling and responses. Curr Opin Plant Biol 16:561–568
• Rampey RA, LeClere S, Kowalczyk M, Ljung K, Sandberg G, Bartel B (2004) A family of auxin-conjugate hydrolases that contributes to free indole-3-acetic acid levels during Arabidopsis germination. Plant Physiol 135:978–988
• Reddy SM, Hitchin S, Melayah D, Pandey AK, Raffier C, Henderson J, Marmeisse R, Gay G (2006) The auxin-inducible GH3 homologue Pp-GH3.16 is downregulated in Pinus pinaster root systems on ectomycorrhizal symbiosis establishment. New Phytol 170:391–400
• Romero-Puertas MC, Corpas FJ, Sandalio LM, Leterrier M, Rodriguez-Serrano M, del Rio LA, Palma JM (2006) Glutathione reductase from pea leaves: response to abiotic stress and characterization of the peroxisomal isozyme. New Phytol 170:43–52
• Roux C, Perrot-Rechenmann C (1997) Isolation by differential display and characterization of a tobacco auxin-responsive cDNA Nt-gh3, related to GH3. FEBS Lett 419:131–136
• Sauer M, Robert S, Kleine-Vehn J (2013) Auxin: simply complicated. J Exp Bot 64:2565–2577
• Slater SM, Yuan HY, Lulsdorf MM, Vandenberg A, Zaharia LI, Han X, Abrams SR (2013) Comprehensive hormone profiling of the developing seeds of four grain legumes. Plant Cell Rep 32:1939–1952
• Sorin C, Negroni L, Balliau T, Corti H, Jacquemot MP, Davanture M, Sandberg G, Zivy M, Bellini C (2006) Proteomic analysis of different mutant genotypes of Arabidopsis led to the identification of 11 proteins correlating with adventitious root development. Plant Physiol 140:349–364
• Staswick PE (2009) The tryptophan conjugates of jasmonic and indole-3-acetic acids are endogenous auxin inhibitors. Plant Physiol 150:1310–1321
• Staswick PE, Tiryaki I, Rowe ML (2002) Jasmonate response locus JAR1 and several related Arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylation. Plant Cell 14:1405–1415
• Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT, Maldonado MC, Suza W (2005) Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17:616–627
• Terol J, Domingo C, Talón M (2006) The GH3 family in plants: genome wide analysis in rice and evolutionary history based on EST analysis. Gene 371:279–290
• Wang H, Tian C-E, Duan J, Wu K (2008) Research progresses on GH3s, one family of primary auxin-responsive genes. Plant Growth Regul 56:225–232
• Westfall CS, Herrmann J, Chen Q, Wang S, Jez JM (2010) Modulating plant hormones by enzyme action: the GH3 family of acyl acid amido synthetases. Plant Signal Behav 5:1607–1612
• Westfall CS, Zubieta C, Herrmann J, Kapp U, Nanao MH, Jez JM (2012) Structural basis for prereceptor modulation of plant hormones by GH3 proteins. Science 336:1708–1711
• Wright RM, Hagen G, Guilfoyle T (1987) An auxin-induced polypeptide in dicotyledonous plants. Plant Mol Biol 9:625–634
• Zhang Z, Li Q, Li Z, Staswick PE, Wang M, Zhu Y, He Z (2007) Dual regulation role of GH3.5 in salicylic acid and auxin signaling during Arabidopsis-Pseudomonas syringae interaction. Plant Physiol 145:450–464

Identyfikatory

DOI

10.1007/s11738-014-1673-y