Tomato yield heterosis is triggered by a dosage sensitivity of the florigen pathway that fine-tunes shoot architecture

Jiang, K., Liberatore, K. L., Park, S. J., Alvarez, J. P., Lippman, Z. B. (2013) Tomato yield heterosis is triggered by a dosage sensitivity of the florigen pathway that fine-tunes shoot architecture. PLoS Genetics, 9 (12). e1004043. ISSN 1553-7390

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URL: http://www.ncbi.nlm.nih.gov/pubmed/24385931
DOI: 10.1371/journal.pgen.1004043

Abstract

The superiority of hybrids has long been exploited in agriculture, and although many models explaining "heterosis" have been put forth, direct empirical support is limited. Particularly elusive have been cases of heterozygosity for single gene mutations causing heterosis under a genetic model known as overdominance. In tomato (Solanum lycopersicum), plants carrying mutations in SINGLE FLOWER TRUSS (SFT) encoding the flowering hormone florigen are severely delayed in flowering, become extremely large, and produce few flowers and fruits, but when heterozygous, yields are dramatically increased. Curiously, this overdominance is evident only in the background of "determinate" plants, in which the continuous production of side shoots and inflorescences gradually halts due to a defect in the flowering repressor SELF PRUNING (SP). How sp facilitates sft overdominance is unclear, but is thought to relate to the opposing functions these genes have on flowering time and shoot architecture. We show that sft mutant heterozygosity (sft/+) causes weak semi-dominant delays in flowering of both primary and side shoots. Using transcriptome sequencing of shoot meristems, we demonstrate that this delay begins before seedling meristems become reproductive, followed by delays in subsequent side shoot meristems that, in turn, postpone the arrest of shoot and inflorescence production. Reducing SFT levels in sp plants by artificial microRNAs recapitulates the dose-dependent modification of shoot and inflorescence production of sft/+ heterozygotes, confirming that fine-tuning levels of functional SFT transcripts provides a foundation for higher yields. Finally, we show that although flowering delays by florigen mutant heterozygosity are conserved in Arabidopsis, increased yield is not, likely because cyclical flowering is absent. We suggest sft heterozygosity triggers a yield improvement by optimizing plant architecture via its dosage response in the florigen pathway. Exploiting dosage sensitivity of florigen and its family members therefore provides a path to enhance productivity in other crops, but species-specific tuning will be required.

Item Type: Paper
Subjects: organs, tissues, organelles, cell types and functions > tissues types and functions > inflorescence
organs, tissues, organelles, cell types and functions > tissues types and functions > meristem
organism description > plant
organism description > plant > tomato
CSHL Authors:
Communities: CSHL labs > Lippman lab
Watson School > Publications
Depositing User: Matt Covey
Date Deposited: 07 Jan 2014 20:15
Last Modified: 23 Sep 2014 13:42
PMCID: PMC3873276
Related URLs:
URI: http://repository.cshl.edu/id/eprint/29206

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