Indole-3-acetylaspartate and indole-3-acetylglutamate, the IAA-amide conjugates in the diploid strawberry achene, are hydrolyzed in growing seedlings
- 161 Downloads
Indole-3-acetylaspartate and indole-3-acetylglutamate are the stored auxin amino acid conjugates of the achene of the diploid strawberry and serve as sources of auxin during seedling growth.
The edible part of the strawberry, a pseudocarp, has long been known to enlarge in response to auxin produced by the developing achenes, the botanical true fruit. Auxin homeostasis involves a complex interaction between biosynthesis, conjugate formation and hydrolysis, catabolism and transport. Strawberry tissues are capable of synthesizing auxin conjugates, and transcriptome data support the expression of genes involved in IAA conjugate formation and hydrolysis throughout embryo development and subsequent seedling growth. Using a highly sensitive and selective mass spectrometric method, we identified all the low molecular weight indole-auxin amino acid conjugates in achenes of F. vesca as consisting of indole-3-acetylaspartate (IAasp) and indole-3-acetylglutamate (IAglu). In contrast to what has been proposed to occur in Arabidopsis, we determined that IAasp and IAglu are hydrolyzed by seedlings to provide a source of free IAA for growth.
KeywordsAuxin conjugates Conjugate hydrolysis IAA amidohydrolase Indole-3-acetic acid Seed auxin precursors Strawberry achenes Woodland strawberry
Liquid chromatography–tandem mass spectrometry
This work was supported by USDA/ARS CRIS 8042-21220-254-00D, by Agriculture and Food Research Initiative competitive awards no. 2018-67011-28056 and 2018-67013-27503 from the USDA National Institute of Food and Agriculture, by the NSF Plant Genome Research Program grant IOS-1238812 as well as support from the Minnesota Agricultural Experiment Station and by the Gordon and Margaret Bailey Endowment for Environmental Horticulture. We thank Paul Fiesel for the synthesis of the [13C6]IAglu used in this study, Dr. Adrian Hegeman for help with figure graphics, and Dr. Laura Shannon for advice on the evolutionary analysis of the IAA amino acid conjugate hydrolases.
- Archbold DD, Dennis FG Jr (1984) Quantification of free ABA and free and conjugated IAA in strawberry achene and receptacle tissue during fruit development. J Am Soc Hort Sci 109:330–335Google Scholar
- Archbold DD, Dennis FG Jr (1985) Strawberry receptacle growth and endogenous IAA content as affected by growth regulator application and achene removal. J Am Soc Hort Sci 110:816–820Google Scholar
- Cohen JD, Baldi BG (1983) Studies of endogenous indole-3-acetyl-l-aspartate during germination of soybeans. Proc Plant Growth Reg Soc Amer 10:117–122Google Scholar
- Cohen JD, Bandurski RS (1982) Chemistry and physiology of the bound auxins. Annu Rev Plant Physiol 33:403–430. https://doi.org/10.1146/annurev.pp.33.060182.002155 Google Scholar
- Denecke J, De Rycke R, Botterman J (1992) Plant and mammalian sorting signals for protein retention in the endoplasmic reticulum contain a conserved epitope. EMBO J 11(6):2345–2355. https://doi.org/10.1002/j.1460-2075.1992.tb05294.x Google Scholar
- Dreher TW, Poovaiah BW (1982) Changes in auxin content during development in strawberry fruits. J Plant Growth Regul 1:267–276Google Scholar
- Edger PP, VanBuren R, Colle M, Poorten TJ, Wai CM, Niederhuth CE, Alger EI, Ou S, Acharya CB, Wang J, Callow P, McKain MR, Shi J, Collier C, Xiong Z, Mower JP, Slovin JP, Hytönen T, Jiang N, Childs KL, Knapp SJ (2018) Single-molecule sequencing and optical mapping yields an improved genome of woodland strawberry (Fragaria vesca) with chromosome-scale contiguity. GigaScience. https://doi.org/10.1093/gigascience/gix124 Google Scholar
- Estrada-Johnson E, Csukasi F, Pizarro CM, Vallarino JG, Kiryakova Y, Vioque A, Brumos J, Medina-Escobar N, Botella MA, Alonso JM, Fernie AR, Sánchez-Sevilla JF, Osorio S, Valpuesta V (2017) Transcriptomic analysis in strawberry fruits reveals active auxin biosynthesis and signaling in the ripe receptacle. Front Plant Sci 8:889. https://doi.org/10.3389/fpls.2017.00889 Google Scholar
- Jung S, Ficklin SP, Lee T, Cheng C-H, Blenda A, Zheng P, Yu J, Bombarely A, Cho I, Ru S, Evans K, Peace C, Abbott AG, Mueller LA, Olmstead MA, Main D (2014) The genome database for Rosaceae (GDR): year 10 update. Nucleic Acids Res 42(D1):D1237–D1244. https://doi.org/10.1093/nar/gkt1012 Google Scholar
- Lis EK (1974) Uptake and metabolism of sucrose-14C and IAA-1-14C in strawberry fruit explants cultivated in vitro (Abstract). In: Antoszewski R, Harrison L, Zych CC, (eds) Proceedings XIX International Horticultural Congress, vol 1A, Warsaw, Poland, 11-18 September. International Society for Horticultural Science, p 61Google Scholar
- Lis EK, Borkowska B, Antoszewski R (1978) Growth regulators in the strawberry fruit. Fruit Sci Rep V(3):17–29Google Scholar
- Morrow EB, Darrow GM, Scott DH (1954) A quick method of cleaning berry seed for breeder. Proc Am Soc Hort Sci 63:265Google Scholar
- Nitsch JP (1950) Growth and morphogenesis of the strawberry as related to auxin. Am J Bot 37(3):211–215. https://doi.org/10.1002/j.1537-2197.1950.tb12183.x Google Scholar
- Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454 Google Scholar
- Sanchez Carranza AP, Singh A, Steinberger K, Panigrahi K, Palme K, Dovzhenko A, Dal Bosco C (2016) Hydrolases of the ILR1-like family of Arabidopsis thaliana modulate auxin response by regulating auxin homeostasis in the endoplasmic reticulum. Sci Rep 6:24212. https://doi.org/10.1038/srep24212 Google Scholar
- Sánchez-Sevilla JF, Vallarino JG, Osorio S, Bombarely A, Posé D, Merchante C, Botella MA, Amaya I, Valpuesta V (2017) Gene expression atlas of fruit ripening and transcriptome assembly from RNA-seq data in octoploid strawberry (Fragaria \( \times \) ananassa). Sci Rep 7:13737. https://doi.org/10.1038/s41598-017-14239-6 Google Scholar
- Yang S, Gao M, Xu C, Gao J, Deshpande S, Lin S, Roe BA, Zhu H (2008) Alfalfa benefits from Medicago truncatula: The RCT1 gene from M. truncatula confers broad-spectrum resistance to anthracnose in alfalfa. Proc Nat Acad Sci USA 105(34):12164–12169. https://doi.org/10.1073/pnas.0802518105 Google Scholar