The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato

Journal name:
Nature Genetics
Volume:
42,
Pages:
459–463
Year published:
DOI:
doi:10.1038/ng.550
Received
Accepted
Published online

Intercrossing different varieties of plants frequently produces hybrid offspring with superior vigor and increased yields, in a poorly understood phenomenon known as heterosis1, 2. One classical unproven model for heterosis is overdominance, which posits in its simplest form that improved vigor can result from a single heterozygous gene3, 4, 5, 6, 7, 8. Here we report that heterozygosity for tomato loss-of-function alleles of SINGLE FLOWER TRUSS (SFT), which is the genetic originator of the flowering hormone florigen, increases yield by up to 60%. Yield overdominance from SFT heterozygosity is robust, occurring in distinct genetic backgrounds and environments. We show that several traits integrate pleiotropically to drive heterosis in a multiplicative manner9, and these effects derive from a suppression of growth termination mediated by SELF PRUNING (SP), an antagonist of SFT. Our findings provide the first example of a single overdominant gene for yield and suggest that single heterozygous mutations may improve productivity in other agricultural organisms.

At a glance

Figures

  1. Heterozygosity for loss-of-function mutations in SFT drives heterosis in tomato.
    Figure 1: Heterozygosity for loss-of-function mutations in SFT drives heterosis in tomato.

    (a) Representative plant and total fruit yield from a high-yielding M82 inbred control plant (left), a low-yielding homozygous loss-of-function mutant allele of SFT (sft-4537, right; Online Methods) and a highly heterotic sft-4537/+ heterozygote (middle). All genotypes are isogenic in the M82 background. (b) Statistical comparison of mean values (± s.e.m.) for total fruit yields between three independently derived sft/sft homozygous mutants (carrying the sft-4537 weak allele, sft-7187 strong allele and sft-stop strong allele, respectively; Online Methods), the inbred M82 control and the F1 sft/+ hybrids of the sft/sft mutants with M82. Total fruit yields from all three sft/+ heterozygotes were heterotic over M82 controls, and sft-4537/+ and sft-7187/+ heterozygotes achieved the same yields as AB2, which is a leading commercial processing-tomato hybrid. (c) Statistical comparison of mean values (± s.e.m.) for fruit sugar content (Brix value) showing an intermediate effect for sft/+ heterozygotes relative to M82 controls (low sugar) and sft/sft homozygotes (high sugar). Lines marked with asterisks are significantly different from the M82 control according to the 'compare with control' (Dunnett's) method: *P < 0.05, **P < 0.01. Similar results were obtained using multiple comparison analysis (Tukey-Kramer test; **P < 0.05) for total fruit yield, which revealed a significant difference between AB2 and sft/+ heterozygotes compared to M82 plants and sft/sft homozygotes. For Brix values, all four groups of genotypes were significantly different from each other (Tukey-Kramer test; **P < 0.05).

  2. sft/+ heterozygosity causes heterosis in distinct genetic backgrounds and growth conditions.
    Figure 2: sft/+ heterozygosity causes heterosis in distinct genetic backgrounds and growth conditions.

    In the tomato industry, genotypes with high yield and Brix value (that is, high values of Brix-yield, the multiplied output of Brix and total fruit yield measured in g/m2) are the most efficient for the production of various tomato concentrates. (a) Statistical comparison of Brix-yield between sft/+ heterozygotes in the background of a full-genome hybrid between M82 and the processing-tomato line E6203 (dark gray) (Online Methods), the homozygous inbred lines M82 and E6203 (white) and the hybrid (M82 × E6203) control (light gray). Experiments were performed in both wide- and dense-spacing conditions (Online Methods). (b) Statistical comparison of Brix-yield between sft/+ heterozygotes in the background of the large-fruited fresh market tomato line M99 (dark gray) (Online Methods), the homozygous inbred lines M82 and M99 (white) and the hybrid controls (M82 × M99) (light gray). The mean values (± s.e.m.) for each genotype marked by asterisks reflect a significant difference from the control hybrids according to the 'compare with control' (Dunnett's) method: *P < 0.05, **P < 0.01. Similar results were obtained using multiple-range means comparison (Tukey-Kramer test; **P < 0.05), which revealed a significant difference between sft/+ heterozygotes and their corresponding controls.

  3. SFT-dependent heterosis arises from multiple phenotypic changes on component traits that integrate to improve yield.
    Figure 3: SFT-dependent heterosis arises from multiple phenotypic changes on component traits that integrate to improve yield.

    (a) Representative inflorescences from M82 plants (left), sft/sft homozygous mutants (right) and sft/+ heterozygotes (middle). The sft/sft homozygotes produce only a few inflorescences before reverting to indeterminate vegetative branches that infrequently produce single fertile flowers, which were counted. Because canonical multiflowered inflorescences almost never form, sft/sft mutant plants have the fewest inflorescences, flowers and fruits of any genotype. (bd) Quantification and statistical comparison of three component traits for yield. (b) sft/+ heterozygotes (dark gray) produce more inflorescences compared to M82 plants. As canonical inflorescences almost never form in sft/sft homozygous mutants, no data was collected for this genotype. (c) sft/+ heterozygotes produce the most flowers per plant of all genotypes (are overdominant) and show an additive effect for fruit weight (d), with a d/[a] value of 0.25. Mean values (± s.e.m.) were compared to the M82 isogenic line (white) using the 'compare with control' (Dunnett's) method when three genotypes were present, and a t-test analysis was performed when two genotypes were present (total inflorescence). Significant differences compared to M82 plants are represented by asterisks: *P < 0.05, **P < 0.01.

  4. Overdominance for inflorescence production is based on a dosage-dependent suppression of growth termination mediated by SP.
    Figure 4: Overdominance for inflorescence production is based on a dosage-dependent suppression of growth termination mediated by SP.

    (a) Temporal accumulation of inflorescences in M82 plants (red) and sft/+ heterozygotes (gray) throughout growth. Significant differences between mean values were calculated in each time point using t-test analyses and are represented by asterisks: *P < 0.05, **P < 0.01. (b) Diagrams showing the reiteration of modular sympodial units along individual shoots from M82-determinate (left), sft/sft homozygote (right) and sft/+ heterozygote plants (middle). Numbers indicate total number of leaves in each sympodial unit, which are indicated by brackets. Flattened gray and black ovals indicate sets of leaves in alternating sympodial units. Black and gray arrows represent axillary shoots preceding the inflorescence in each sympodial unit. Note that there are more sympodial units, inflorescences and leaves along each shoot of sft/+ heterozygotes compared to M82-determinate and sft/sft mutant plants (Supplementary Fig. 4). (c) Diagram of a shoot from an M82-indeterminate plant (left) and a yield comparison between sft/+ heterozygotes in an indeterminate background (sft/+, sp/+) and control M82-indeterminate plants (sft/+, sp/+). Total fruit yields of M82-determinate × M82-indeterminate (light gray) and sft/sft × M82-indeterminate (dark gray) do not differ significantly from each other, and both are lower yielding than the heterotic sft/+ M82-determinate plants, which are the highest yielding of all genotypes (Supplementary Fig. 5). (d) RT-PCR analysis of SFT and Sl-AP1 expression levels in young expanding leaves and shoot apices, respectively, showing no qualitative differences in transcript accumulation between M82 plants and heterozygote genotypes for either gene. EXP (EXPRESSED, SGN-U346908) is a published gene showing stable expression across diverse tissues, used here as real-time PCR control (Online Methods).

Accession codes

Referenced accessions

NCBI Reference Sequence

References

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Author information

Affiliations

  1. The Hebrew University of Jerusalem Faculty of Agriculture, Institute of Plant Sciences, Rehovot, Israel.

    • Uri Krieger &
    • Dani Zamir
  2. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA.

    • Zachary B Lippman

Contributions

U.K., Z.B.L. and D.Z. planned and carried out all experiments, collected the data, performed the statistical analyses and wrote the paper.

Competing financial interests

D.Z. is a cofounder of Phenom Networks, a privately held company that is serving as a repository and online statistical analysis platform for the raw heterosis field data.

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