Divergence in the Enzymatic Activities of a Tomato and Solanum pennellii Alcohol Acyltransferase Impacts Fruit Volatile Ester Composition.

Tomato fruits accumulate a diverse set of volatiles including multiple esters. The content of ester volatiles is relatively low in tomato fruits (Solanum lycopersicum) and far more abundant in the closely related species S. pennellii. There are also qualitative variations in ester content between the two species. We have previously shown that high expression of a non-specific esterase is critical for the low overall ester content of S. lycopersicum fruit relative to S. pennellii fruit. Here, we show that qualitative differences in ester composition are the consequence of divergence in enzymatic activity of a ripening-related alcohol acyltransferase (AAT1). The S. pennellii AAT1 is more efficient than the tomato AAT1 for all the alcohols tested. The two enzymes have differences in their substrates preferences that explain variations observed in the volatiles. Together, the results illustrate how two related species have evolved to precisely adjust their volatile content by modulating the balance of synthesis and degradation of esters.

[1]  D. Chagné,et al.  The AAT1 locus is critical for the biosynthesis of esters contributing to 'ripe apple' flavour in 'Royal Gala' and 'Granny Smith' apples. , 2014, The Plant journal : for cell and molecular biology.

[2]  A. Granell,et al.  The expanded tomato fruit volatile landscape. , 2013, Journal of experimental botany.

[3]  Jinhe Bai,et al.  Identification of a strawberry flavor gene candidate using an integrated genetic-genomic-analytical chemistry approach , 2014, BMC Genomics.

[4]  Koichiro Tamura,et al.  MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. , 2013, Molecular biology and evolution.

[5]  H. Klee,et al.  Better Fruits and Vegetables through Sensory Analysis , 2013, Current Biology.

[6]  H. Klee,et al.  Genetic challenges of flavor improvement in tomato. , 2013, Trends in genetics : TIG.

[7]  R. Herrera,et al.  Structural analysis of the alcohol acyltransferase protein family from Cucumis melo shows that enzyme activity depends on an essential solvent channel , 2013, The FEBS journal.

[8]  H. Klee,et al.  Role of an esterase in flavor volatile variation within the tomato clade , 2012, Proceedings of the National Academy of Sciences.

[9]  W. Schwab,et al.  The fruit ripening-related gene FaAAT2 encodes an acyl transferase involved in strawberry aroma biogenesis. , 2012, Journal of experimental botany.

[10]  Peter Bliss,et al.  The Chemical Interactions Underlying Tomato Flavor Preferences , 2012, Current Biology.

[11]  Daniel W. A. Buchan,et al.  The tomato genome sequence provides insights into fleshy fruit evolution , 2012, Nature.

[12]  Functional allelic diversity of the apple alcohol acyl-transferase gene MdAAT1 associated with fruit ester volatile contents in apple cultivars , 2012, Molecular Breeding.

[13]  R. Newcomb,et al.  Characterisation of two alcohol acyltransferases from kiwifruit (Actinidia spp.) reveals distinct substrate preferences. , 2011, Phytochemistry.

[14]  Robert M. Buels,et al.  The Sol Genomics Network (solgenomics.net): growing tomatoes using Perl , 2010, Nucleic Acids Res..

[15]  H. Klee Improving the flavor of fresh fruits: genomics, biochemistry, and biotechnology. , 2010, The New phytologist.

[16]  J. Pech,et al.  VpAAT1, a gene encoding an alcohol acyltransferase, is involved in ester biosynthesis during ripening of mountain papaya fruit. , 2010, Journal of agricultural and food chemistry.

[17]  D. Warren,et al.  Ecological and geographic modes of species divergence in wild tomatoes. , 2010, American journal of botany.

[18]  Yang Zhang,et al.  I-TASSER: a unified platform for automated protein structure and function prediction , 2010, Nature Protocols.

[19]  R. Herrera,et al.  Aroma development during ripening of Fragaria chiloensis fruit and participation of an alcohol acyltransferase (FcAAT1) gene. , 2009, Journal of agricultural and food chemistry.

[20]  J. Carlson,et al.  Priming defense genes and metabolites in hybrid poplar by the green leaf volatile cis-3-hexenyl acetate. , 2008, The New phytologist.

[21]  E. Baldwin,et al.  Interaction of volatiles, sugars, and acids on perception of tomato aroma and flavor descriptors. , 2008, Journal of food science.

[22]  J. Gershenzon,et al.  Characterization of a BAHD acyltransferase responsible for producing the green leaf volatile (Z)-3-hexen-1-yl acetate in Arabidopsis thaliana. , 2007, The Plant journal : for cell and molecular biology.

[23]  D. Kourkoutas,et al.  Comparison of the volatile compositions and flavour properties of cantaloupe, Galia and honeydew muskmelons , 2006 .

[24]  Jie Liang,et al.  CASTp: computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues , 2006, Nucleic Acids Res..

[25]  J. D’Auria Acyltransferases in plants: a good time to be BAHD. , 2006, Current opinion in plant biology.

[26]  De-quan Li,et al.  Molecular cloning and expression of a gene encoding alcohol acyltransferase (MdAAT2) from apple (cv. Golden Delicious). , 2006, Phytochemistry.

[27]  Hiroshi Ezura,et al.  A highly efficient transformation protocol for Micro-Tom, a model cultivar for tomato functional genomics. , 2006, Plant & cell physiology.

[28]  P. Bliss,et al.  Identification of loci affecting flavour volatile emissions in tomato fruits. , 2006, Journal of experimental botany.

[29]  P. Oeller,et al.  Plant Volatile Compounds: Sensory Cues for Health and Nutritional Value? , 2006 .

[30]  Xinlu Chen,et al.  Generation of Phenylpropanoid Pathway-Derived Volatiles in Transgenic Plants: Rose Alcohol Acetyltransferase Produces Phenylethyl Acetate and Benzyl Acetate in Petunia Flowers , 2006, Plant Molecular Biology.

[31]  Jihong Wang,et al.  The biosynthesis and regulation of biosynthesis of Concord grape fruit esters, including 'foxy' methylanthranilate. , 2005, The Plant journal : for cell and molecular biology.

[32]  J. Pech,et al.  Functional Characterization of a Melon Alcohol Acyl-transferase Gene Family Involved in the Biosynthesis of Ester Volatiles. Identification of the Crucial Role of a Threonine Residue for Enzyme Activity* , 2005, Plant Molecular Biology.

[33]  U. Ravid,et al.  Developmental and varietal differences in volatile ester formation and acetyl-CoA: alcohol acetyl transferase activities in apple (Malus domestica Borkh.) fruit. , 2005, Journal of agricultural and food chemistry.

[34]  R. Newcomb,et al.  An alcohol acyl transferase from apple (cv. Royal Gala), MpAAT1, produces esters involved in apple fruit flavor , 2005, The FEBS journal.

[35]  Beverly A. Underwood,et al.  Circadian Regulation of the PhCCD1 Carotenoid Cleavage Dioxygenase Controls Emission of β-Ionone, a Fragrance Volatile of Petunia Flowers1 , 2004, Plant Physiology.

[36]  Conrad C. Huang,et al.  UCSF Chimera—A visualization system for exploratory research and analysis , 2004, J. Comput. Chem..

[37]  A. Aharoni,et al.  Functional Characterization of Enzymes Forming Volatile Esters from Strawberry and Banana[w] , 2004, Plant Physiology.

[38]  J. Tumlinson,et al.  Airborne signals prime plants against insect herbivore attack. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[39]  S. Tanksley,et al.  Genetic variation inSolanum pennellii: Comparisons with two other sympatric tomato species , 1981, Plant Systematics and Evolution.

[40]  E. Pichersky,et al.  Volatile Ester Formation in Roses. Identification of an Acetyl-Coenzyme A. Geraniol/Citronellol Acetyltransferase in Developing Rose Petals1 , 2003, Plant Physiology.

[41]  Hilko van der Voet,et al.  Identification of the SAAT Gene Involved in Strawberry Flavor Biogenesis by Use of DNA Microarrays , 2000, Plant Cell.

[42]  D. Grierson,et al.  Ethylene and developmental signals regulate expression of lipoxygenase genes during tomato fruit ripening , 1999 .

[43]  D. Zamir,et al.  An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. , 1995, Genetics.

[44]  C. Sanz,et al.  Aroma components and free amino acids in strawberry variety Chandler during ripening , 1992 .

[45]  S. Warnock Natural Habitats of Lycopersicon Species , 1991 .

[46]  C. Macku,et al.  Production of volatiles by ripening bananas , 1987 .