Tomato facultative parthenocarpy results from SlAGAMOUS-LIKE 6 loss of function.

Chen Klap,Anthony M Bolger,Yehiam Salts,Ester Yeshayahou,Björn Usadel,Rivka Barg,Suresh K Gupta,Sara Shabtai,Tzahi Arazi

doi:10.1111/pbi.12662

Chen Klap, Anthony M Bolger + Show 7 more

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https://doi.org/10.1111/pbi.12662

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Abstract

SummaryThe extreme sensitivity of the microsporogenesis process to moderately high or low temperatures is a major hindrance for tomato (Solanum lycopersicum) sexual reproduction and hence year‐round cropping. Consequently, breeding for parthenocarpy, namely, fertilization‐independent fruit set, is considered a valuable goal especially for maintaining sustainable agriculture in the face of global warming. A mutant capable of setting high‐quality seedless (parthenocarpic) fruit was found following a screen of EMS‐mutagenized tomato population for yielding under heat stress. Next‐generation sequencing followed by marker‐assisted mapping and CRISPR/Cas9 gene knockout confirmed that a mutation in SlAGAMOUS‐LIKE 6 (SlAGL6) was responsible for the parthenocarpic phenotype. The mutant is capable of fruit production under heat stress conditions that severely hamper fertilization‐dependent fruit set. Different from other tomato recessive monogenic mutants for parthenocarpy, Slagl6 mutations impose no homeotic changes, the seedless fruits are of normal weight and shape, pollen viability is unaffected, and sexual reproduction capacity is maintained, thus making Slagl6 an attractive gene for facultative parthenocarpy. The characteristics of the analysed mutant combined with the gene's mode of expression imply SlAGL6 as a key regulator of the transition between the state of ‘ovary arrest’ imposed towards anthesis and the fertilization‐triggered fruit set.

Highlights

Fruit development following fertilization is critical for the completion of the plant life cycle
Sexual reproduction entails that the hypersensitivity of the microsporogenesis process, and the mature male gametes to moderately high or low temperatures, and to extreme humidity or light intensity (El Ahmadi and Stevens, 1979; Mesihovic et al, 2016; Picken, 1984; Sato et al, 2006), is a major hindrance for year-round fertilization-dependent tomato yielding
We demonstrate that mutated alleles of the MADS-box gene SlAGAMOUS-LIKE 6 (SlAGL6) enable tomato yielding under heat stress

Summary

Introduction

Fruit development following fertilization is critical for the completion of the plant life cycle. If fertilization is successfully completed, a signal believed to be produced by the young embryo provokes the ovary to resume growth. This growth involves initially a phase of rapid cell division and expansion (designated phase II or ‘fruit set’) for 5–10 days (Bohner and Bangerth, 1988; Varga and Bruinsma, 1986), and subsequently (during phase III) growth is driven mainly by cell enlargement concomitant with nuclear polyploidization (Chevalier et al, 2014, and references therein). The default programme of fertilization-dependent fruit development ensures that resources are not wasted sustaining purposeless fruit development, whereas parthenocarpy, that is fertilization-independent seedless fruit development, is a counterproductive trait in all the sexually reproducing plant species. Other advantages of parthenocarpy relate to consumers’ preference of seedless over seeded fruits, improved fruit quality due to elevated content of total soluble solids (TSS) (Carmi et al, 2003; Casas Diaz et al, 1987; Falavigna et al, 1978; Ficcadenti et al, 1999) and saving of energy invested in separating the seeds from processed products

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