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

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Authors
Charles Goulet, Yusuke Kamiyoshihara, Nghi B. Lam, Théo Richard, Mark G. Taylor, Denise M. Tieman, Harry J. Klee
Year
2015
DOI
10.1016/j.molp.2014.11.007
Subject
Molecular Biology / Plant Science

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lc e i B -06 cl is relatively low in tomato fruits (Solanum lycopersicum) and far more abundant in the closely related spe-cies Solanum 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 substrate preferences that explain the variations observed in the volatiles. The results illustrate how two related species have evolved to precisely adjust their volatile content by modulating the balance of the synthesis and degradation of esters.

Key words: volatiles, Solanum lycopersicum, evolution, SlAAT1, SpAAT1

Goulet C., Kamiyoshihara Y., Lam N.B., Richard T., Taylor M.G., Tieman D.M., and Klee H.J. (2015).

Divergence in the Enzymatic Activities of a Tomato and Solanum pennellii Alcohol Acyltransferase Impacts Fruit

Volatile Ester Composition. Mol. Plant. 8, 153–162.

INTRODUCTION

The unique flavors of different fruits are, in large part, dependent on complex blends of organic volatile compounds (Klee, 2010).

Volatile content is likely the result of selection pressures based on several factors including attraction of seed-dispersing agents and defense against herbivores and pathogens. The unique fruit aroma of each species, even within a genus, is therefore a complex evolutionary process involving multiple metabolic pathways, fine tuned to the environmental pressures faced by that species.

The volatiles of the tomato fruit are mostly derived from amino acids, fatty acids, and carotenoid precursors (Baldwin et al., 2008; Rambla et al., 2014). Individually, these compounds smell nothing like tomato but together they form the typical aroma of tomato that we have learned to love (Goff and Klee, 2006;

Bartoshuk and Klee, 2013). From a human perspective, some of these volatiles affect our preference while others have little or no influence on liking. Consumer preference panels conducted with a large, diverse set of tomato varieties identified volatiles

Volatile esters contribute to the characteristic aroma of many fruits and flowers. Their aromas are generally described as fruity or floral-like. Examples of species accumulating a significant amount of esters in their fruits or flowers include banana, apple, rose, melon, and strawberry (Macku and Jennings, 1987; Perez et al., 1992; Shalit et al., 2003; Holland et al., 2005; Kourkoutas et al., 2006). Volatile esters are also found in vegetative tissues of most species. cis-3-Hexenyl acetate, for example, is one of the most abundant volatiles emitted from mechanically or herbivore-damaged Arabidopsis thaliana plants (D’Auria et al., 2007) and can prime a defense response in surrounding plants (Engelberth et al., 2004; Frost et al., 2008). These results are consistent with a role for esters in plant defense and plantto-plant signaling. Volatile esters are produced by alcohol acyltransferases that catalyze esterification of an acyl moiety from an acyl-coenzyme A (acyl-CoA) donor onto an alcohol.

The widely distributed acetate esters are formed with acetylCoA (2 carbons), while butyrate esters or hexanoate are derived from butyryl-CoA (4 carbons) and hexanoyl-CoA (6 carbons),Divergence in theEnzyma and Solanum pennellii A

Impacts Fruit Volatile Est

Charles Goulet1, Yusuke Kamiyoshihara2, Ngh

Denise M. Tieman2 and Harry J. Klee2,* 1De´partement de Phytologie, Universite´ Laval, Que´bec, QC G1V 0A6, Canada 2Horticultural Sciences Department, University of Florida, Gainesville, FL 32611 *Correspondence: Harry J. Klee (hjklee@ufl.edu) http://dx.doi.org/10.1016/j.molp.2014.11.007

ABSTRACT

Tomato fruits accumulate a diverse set of volatiles in

Molecular Plant

Research Articlethat are positively or negatively correlated with human preferences (Tieman et al., 2012). Among them, individual acetate esters as well as total acetate esters are negatively correlated with preference (Goulet et al., 2012).

MticActivitiesofaTomato ohol Acyltransferase r Composition . Lam2, The´o Richard1, Mark G. Taylor2, 90, USA uding multiple esters. The content of ester volatilesPublished by the Molecular Plant Shanghai Editorial Office in association with

Cell Press, an imprint of Elsevier Inc., on behalf of CSPB and IPPE, SIBS, CAS. olecular Plant 8, 153–162, January 2015 ª The Author 2015. 153

Analysis of the tomato genome (Tomato Genome Consortium, da) ) ewe llea umi mis sis) a) nas

AT

T4 osa (Fra (Frarespectively. Acetate esters are the only volatile esters easily detectable in the tomato fruit, with the exception of methyl salicylate, which is formed by an O-methyltransferase rather than an alcohol acyltransferase (Goulet et al., 2012; Tieman et al., 2012).

SlAAT3

SlAAT4

BPBT (Petunia x hybri

CmAAT3 (Cucumis melo

CbBEBT (Clarkia br

VpAAT1 (Vasconce

CmAAT1 (Cuc

CmAAT2 (Cucu

AcAT16 (Actinidia chinen

AeAT9 (Actinidia erianth

FaAAT2 (Fragaria x ana

MpAAT1 (Malus pumila)

MdAAT2 (Malus pumila)

SlAAT1

SpAAT1

SlAAT5

SlAAT2

BanA

CbBEAT (Clarkia breweri)

CmAA

RhAAT (R

VAAT

SAAT100 100 100 100 99 100 100 40 100 100 99 100 96 86 90 99 89 99 40 91 0,5

Molecular PlantIn contrast to the fruits of many species, volatile ester levels are relatively low in tomato fruit. We previously showed that high expression of an esterase gene (SlCXE1) is one of the major determinants of low acetate ester accumulation in ripe tomato fruits (Goulet et al., 2012). The tomato clade can be divided into two subgroups based on fruit characteristics: the red-fruited group and the green-fruited group. The red-fruited species of the clade have relatively low fruit acetate ester content while the greenfruited species accumulate much higher fruit acetate ester levels.