Modulating auxin response stabilizes tomato fruit set

Author:

Israeli Alon1ORCID,Schubert Ramona2ORCID,Man Nave1,Teboul Naama1ORCID,Serrani Yarce Juan Carlos3ORCID,Rosowski Emily E3ORCID,Wu Miin-Feng3ORCID,Levy Matan1ORCID,Efroni Idan1ORCID,Ljung Karin4ORCID,Hause Bettina2ORCID,Reed Jason W3ORCID,Ori Naomi1ORCID

Affiliation:

1. The Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture, Hebrew University , PO Box 12, Rehovot 76100 , Israel

2. Department of Cell and Metabolic Biology, Leibniz Institute of Plant Biochemistry , Halle 06120 , Germany

3. Department of Biology, University of North Carolina at Chapel Hill , Chapel Hill, NC 27599-3280 , USA

4. Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences , Umeå 901 83 , Sweden

Abstract

Abstract Fruit formation depends on successful fertilization and is highly sensitive to weather fluctuations that affect pollination. Auxin promotes fruit initiation and growth following fertilization. Class A auxin response factors (Class A ARFs) repress transcription in the absence of auxin and activate transcription in its presence. Here, we explore how multiple members of the ARF family regulate fruit set and fruit growth in tomato (Solanum lycopersicum) and Arabidopsis thaliana, and test whether reduction of SlARF activity improves yield stability in fluctuating temperatures. We found that several tomato Slarf mutant combinations produced seedless parthenocarpic fruits, most notably mutants deficient in SlARF8A and SlARF8B genes. Arabidopsis Atarf8 mutants deficient in the orthologous gene had less complete parthenocarpy than did tomato Slarf8a Slarf8b mutants. Conversely, Atarf6 Atarf8 double mutants had reduced fruit growth after fertilization. AtARF6 and AtARF8 likely switch from repression to activation of fruit growth in response to a fertilization-induced auxin increase in gynoecia. Tomato plants with reduced SlARF8A and SlARF8B gene dosage had substantially higher yield than the wild type under controlled or ambient hot and cold growth conditions. In field trials, partial reduction in the SlARF8 dose increased yield under extreme temperature with minimal pleiotropic effects. The stable yield of the mutant plants resulted from a combination of early onset of fruit set, more fruit-bearing branches and more flowers setting fruits. Thus, ARF8 proteins mediate the control of fruit set, and relieving this control with Slarf8 mutations may be utilized in breeding to increase yield stability in tomato and other crops.

Funder

US-Israel Binational Agricultural Research and Development Fund

(BARD)

USDA NRI

Deutsche Forschungsgemeinschaft

(DFG)

Israel Science Foundation

Azrieli Foundation

Swedish Governmental Agency for Innovation Systems

(VINNOVA)

Swedish Research Council

(Vetenskapsrådet )

Publisher

Oxford University Press (OUP)

Subject

Plant Science,Genetics,Physiology

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