A TILLING allele of the tomato Aux/IAA9 gene offers new insights into fruit set mechanisms and perspectives for breeding seedless tomatoes

Mazzucato, Andrea; Cellini, Francesco; Bouzayen, Mondher; Zouine, Mohamed; Mila, Isabelle; Minoïa, Silvia; Petrozza, Angelo; Picarella, Maurizio Enea; Ruiu, Fabrizio; Carriero, Filomena

doi:10.1007/s11032-015-0222-8

Cited by 62 publications

(45 citation statements)

References 56 publications

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“…6 ) further supports the positive role of auxin on sugar metabolism in tomato fruits. In agreement with our findings, fruits of an Aux/IAA9 frame-shift tomato mutant identified via TILLING-based screening exhibited an increased brix value compared to the WT in the fully ripe stage under either greenhouse or open-field conditions 57 . Therefore, although the direct regulation of tomato AGPase , LIN and SUT genes by light signaling-associated transcription factors also cannot be excluded due to the presence of HY5 and/or PIF bindings motifs in their promoter regions, it seems plausible to hypothesize that the reduced sugar content and transcript abundance of sink- and starch biosynthesis-related genes observed in early developing au fruits may be associated with the lower cytokinin and auxin signaling output detected in this PΦB-deficient mutant compared to the WT.…”

Section: Discussionsupporting

confidence: 91%

Phytochromobilin deficiency impairs sugar metabolism through the regulation of cytokinin and auxin signaling in tomato fruits

Bianchetti

Cruz

Oliveira

et al. 2017

Sci Rep

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Phytochomes and plant hormones have been emerging as important regulators of fleshy fruit biology and quality traits; however, the relevance of phytochrome-hormonal signaling crosstalk in controlling fruit development and metabolism remains elusive. Here, we show that the deficiency in phytochrome chromophore phytochromobilin (PΦB) biosynthesis inhibits sugar accumulation in tomato (Solanum lycopersicum) fruits by transcriptionally downregulating sink- and starch biosynthesis-related enzymes, such as cell-wall invertases, sucrose transporters and ADP-glucose pyrophosphorylases. PΦB deficiency was also shown to repress fruit chloroplast biogenesis, which implicates more limited production of photoassimilates via fruit photosynthesis. Genetic and physiological data revealed the involvement of auxins and cytokinins in mediating the negative impact of PΦB deficiency on fruit sink strength and chloroplast formation. PΦB deficiency was shown to transcriptionally repress type-A TOMATO RESPONSE REGULATORs and AUXIN RESPONSE FACTORs both in pericarp and columella, suggesting active phytochrome-hormonal signaling crosstalk in these tissues. Data also revealed that PΦB deficiency influences fruit ripening by delaying the climacteric rise in ethylene production and signaling. Altogether, the data uncover the impact of phytochromobilin deficiency in fine-tuning sugar metabolism, chloroplast formation and the timing of fruit ripening and also reveal a link between auxins, cytokinins and phytochromes in regulating sugar import and accumulation in fruits.

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Section: Discussionsupporting

confidence: 91%

Phytochromobilin deficiency impairs sugar metabolism through the regulation of cytokinin and auxin signaling in tomato fruits

Bianchetti

Cruz

Oliveira

et al. 2017

Sci Rep

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“…Since tomato and other vegetables that could benefit from parthenocarpy are commonly propagated from seeds, hence only genetic sources for facultative parthenocarpy, where seeded fruits can develop following successful fertilization (Varoquaux et al, 2000), are of practical value. Presently, the most extensively characterized nontransgenic sources for facultative parthenocarpy in tomato are as follows: the three monogenic sources, pat (Beraldi et al, 2004; presumably a mutated Solyc03g120910, Selleri, 2011;Soressi and Salamini, 1975), procera (a mutated SlDELLA, Bassel et al, 2008) and entire (mutated SlAUX/IAA9, Mazzucato et al, 2015;Saito et al, 2011), all of which manifest undesired pleiotropic effects; and the three digenic sources, pat-2 (Hazra and Dutta, 2010;Vardy et al, 1989), IL5-1 and IVT-line 1 (Gorguet et al, 2008), all manifesting acceptable parthenocarpic phenotype; and the inferior oligogenic source pat-3/pat-4 (Nuez et al, 1986;Philouze and Maisonneuve, 1978). Despite the importance of this trait, exploitation of these mutants in breeding programmes is still rather limited.…”

Section: Introductionmentioning

confidence: 99%

Tomato facultative parthenocarpy results from SlAGAMOUS‐LIKE 6 loss of function

Klap

Yeshayahou

Bolger

et al. 2016

Plant Biotechnology Journal

253

131

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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.

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“…For instance, fruits from the entire mutant are parthenocarpic due to the lack of SlIAA9 function. SlIAA9 belongs to Aux/IAA gene family, and its downregulation in entire indicates that SlIAA9 is important to mediate auxin responses during fruit set (Wang et al, 2005;Zhang et al, 2007;Mazzucato et al, 2015). Parthenocarpy in tomato pat mutants is associated with high levels of active GA in non-pollinated ovary due to misexpression of GA metabolism-associated genes (Fos et al, 2000;Olimpieri et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

microRNA159‐targeted SlGAMYB transcription factors are required for fruit set in tomato

Silva

Bidoia

et al. 2017

The Plant Journal

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The transition from flowering to fruit production, namely fruit set, is crucial to ensure successful sexual plant reproduction. Although studies have described the importance of hormones (i.e. auxin and gibberellins) in controlling fruit set after pollination and fertilization, the role of microRNA-based regulation during ovary development and fruit set is still poorly understood. Here we show that the microRNA159/GAMYB1 and -2 pathway (the miR159/GAMYB1/2 module) is crucial for tomato ovule development and fruit set. MiR159 and SlGAMYBs were expressed in preanthesis ovaries, mainly in meristematic tissues, including developing ovules. SlMIR159-overexpressing tomato cv. Micro-Tom plants exhibited precocious fruit initiation and obligatory parthenocarpy, without modifying fruit shape. Histological analysis showed abnormal ovule development in such plants, which led to the formation of seedless fruits. SlGAMYB1/2 silencing in SlMIR159-overexpressing plants resulted in misregulation of pathways associated with ovule and female gametophyte development and auxin signalling, including AINTEGUMENTA-like genes and the miR167/SlARF8a module. Similarly to SlMIR159-overexpressing plants, SlGAMYB1 was downregulated in ovaries of parthenocarpic mutants with altered responses to gibberellins and auxin. SlGAMYBs likely contribute to fruit initiation by modulating auxin and gibberellin responses, rather than their levels, during ovule and ovary development. Altogether, our results unveil a novel function for the miR159-targeted SlGAMYBs in regulating an agronomically important trait, namely fruit set.

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A TILLING allele of the tomato Aux/IAA9 gene offers new insights into fruit set mechanisms and perspectives for breeding seedless tomatoes

Abstract: A TILLING allele of the tomato Aux/IAA9 gene offers new insights into fruit set mechanisms and perspectives for breeding seedless tomatoes. (2015) Molecular Breeding, vol. 35 (n° 1).

Cited by 62 publications

References 56 publications

Phytochromobilin deficiency impairs sugar metabolism through the regulation of cytokinin and auxin signaling in tomato fruits

Phytochromobilin deficiency impairs sugar metabolism through the regulation of cytokinin and auxin signaling in tomato fruits

Tomato facultative parthenocarpy results from SlAGAMOUS‐LIKE 6 loss of function

microRNA159‐targeted SlGAMYB transcription factors are required for fruit set in tomato

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