volatiles due to the loss of a single superior allele
may not be apparent to an individual making selections, but cumulative loss of superior alleles
affecting many volatiles has resulted in overall
flavor deterioration over many breeding cycles.
However, content of desirable chemicals can be
increased, and content of undesirable chemicals
decreased, by utilizing molecular markers associated with superior alleles.
Replacement of undesirable alleles should have
a strong positive effect on consumer liking. Since
volatiles are active at picomolar to nanomolar con-
centrations, substantial increases in their contents
can be achieved with minimal metabolic penalty
and less yield drag. However, sugars, which corre-
late highly with consumer liking, are present in
millimolar concentrations, so increasing their con-
tent will only be achievable at the cost of reduced
fruit size. We identified multiple loci with potential
for increasing fruit sugar content. For example,
reintroduction of the alternate Lin5 should result
in higher sugar content. Although in most cases,
higher sugar content is associated with a reduction
in the size of a fruit, consumers do not prefer large
fruit and are very willing to purchase minimally
smaller fruit with superior taste (16). One possible
solution to this trade-off between higher sugar and
smaller size is based on our observations that cer-
tain fruit volatiles significantly enhance the percep-
tion of sweetness (2, 5). Notably, large effects on
perceived sweetness are conferred by apocarote-
noid volatiles. The selection of alleles associated
with higher apocarotenoid content that are iden-
tified here can potentially improve perceived sweet-
ness without negatively affecting fruit size.
Modern commercial tomatoes do not have the
flavor of older varieties. Although postharvest practices, such as refrigeration, can irreversibly damage
flavor, making improvements in flavor-associated
chemicals is the first step to restoring the potential
of widely grown commercial varieties. Our results
provide a roadmap for improvement of flavor. The
genes and pathways identified here in the tomato
almost certainly point to pathways worth investigating for improvement of flavor quality in other
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This work was supported by the NSF (grant IOS-0923312 to H.K.),
the China National Key Research and Development Program for
Crop Breeding (grant 2016YFD0100307 to S.H.), the Leading
Talents of Guangdong Province Program (grant 00201515 to S.H.),
the National Natural Science Foundation of China (grant 31601756
to G.Z.), the European Research Council (grant ERC-2011-AdG
294691 YIELD to D.Z.), and the European Commission Horizon
2020 program (TRADITOM grant 634561 to A.G. and D.Z.) This
work was also supported by the Chinese Academy of Agricultural
Science (ASTIP–CAAS) and the Shenzhen municipal and Dapeng
district governments. We acknowledge the assistance of L. Kates in
fieldwork and volatile, sugar, and acid quantification.
Materials and Methods
Figs. S1 to S25
Tables S1 to S8
6 October 2016; accepted 22 December 2016
394 27 JANUARY 2017 • VOL 355 ISSUE 6323 sciencemag.org SCIENCE
Fig. 3. Combinations
2-one (MHO) and
alleles found in
S. lycopersicum var
varieties. In all panels,
R is the reference
(Heinz 1706) allele, and
A is the alternate allele.
(A) Allele distribution of
MHO loci at positions
S. lycopersicum var
(B) Allele distribution in
varieties containing R
or A allele combinations
loci located at
chr11:7652084 were chosen. (C) Mean (±SE) MHO content in varieties containing the indicated allele combinations. (D) Mean (±SE) geranylacetone content in
the indicated allele combinations. The two most abundant allele combinations in modern varieties are indicated in (C) and (D) in red. Letters in (C) and (D)
indicate separations as determined by pairwise Student’s t test, where bars with no shared letters indicate a statistically significant difference in volatile contents
between the data sets.