Major Impacts of Widespread Structural Variation on Gene Expression and Crop Improvement in Tomato

Alonge, Michael; Wang, Xingang; Benoit, Matthias; Soyk, Sebastian; Pereira, Lara; Zhang, Lei; Suresh, Hamsini; Ramakrishnan, S.; Maumus, Florian; Ciren, Danielle; Levy, Yuval; Harel, Tom; Shalev-Schlosser, Gili; Amsellem, Ziva; Razifard, Hamid; Caicedo, Ana L.; Tieman, Denise M.; Klee, Harry J.; Kirsche, Melanie; Aganezov, Sergey; Ranallo-Benavidez, T. Rhyker; Lemmon, Zachary H.; Kim, Jennifer; Robitaille, Gina; Kramer, Melissa; Goodwin, Sara; McCombie, W. Richard; Hutton, Samuel F.; Eck, Joyce Van; Gillis, Jesse; Eshed, Yuval; Sedlazeck, Fritz J.; Knaap, Esther van der; Schatz, Michael C.; Lippman, Zachary B.

doi:10.1016/j.cell.2020.05.021

Cited by 597 publications

(664 citation statements)

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“…These gains will in turn translate to cost savings for resequencing and validation experiments. Indeed, SVCollector has already been applied to larger sequencing projects such as a detailed study of 11 human genomes and 100 tomato genomes sequenced with long reads (Shafin et al 2020;Alonge et al 2020).…”

Section: Discussionmentioning

confidence: 99%

SVCollector: Optimized sample selection for cost-efficient long-read population sequencing

Ranallo-Benavidez

Lemmon

Soyk

et al. 2020

Preprint

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An increasingly important scenario in population genetics is when a large cohort has been genotyped using a low-resolution approach (e.g. microarrays, exome capture, short-read WGS), from which a few individuals are selected for resequencing using a more comprehensive approach, especially long-read sequencing. The subset of individuals selected should ensure that the captured genetic diversity is fully representative and includes variants across all subpopulations. For example, human variation has historically been focused on individuals with European ancestry, but this represents a small fraction of the overall diversity.To address this goal, SVCollector (https://github.com/fritzsedlazeck/SVCollector) identifies the optimal subset of individuals for resequencing. SVCollector analyzes a population-level VCF file from a low resolution genotyping study. It then computes a ranked list of samples that maximizes the total number of variants present from a subset of a given size. To solve this optimization problem, SVCollector implements a fast greedy heuristic and an exact algorithm using integer linear programming. We apply SVCollector on simulated data, 2504 human genomes from the 1000 Genomes Project, and 3024 genomes from the 3K Rice Genomes Project and show the rankings it computes are more representative than widely used naive strategies. Notably, we show that when selecting an optimal subset of 100 samples in these two cohorts, SV-Collector identifies individuals from every subpopulation while naive methods yield an unbalanced selection. Finally, we show the number of variants present in cohorts of different sizes selected using this approach follows a power-law distribution that is naturally related to the population genetic concept of the allele frequency spectrum, allowing us to estimate the diversity present with increasing numbers of samples.

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Section: Discussionmentioning

confidence: 99%

SVCollector: Optimized sample selection for cost-efficient long-read population sequencing

Ranallo-Benavidez

Lemmon

Soyk

et al. 2020

Preprint

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“…Because of their importance for plant development, it is also possible that FUL-like genes have played a role during tomato domestication. This has already been unveiled for the MADS-box genes JOINTLESS 2 (J2, also called SlMBP21), ENHANCER OF JOINTLESS2 (EJ2/MADS1, hereafter called EJ2) and SISTER OF TOMATO MADS-box gene 3 (STM3) (Roldan et al, 2017;Soyk et al, 2017;Soyk et al, 2019;Alonge et al, 2020). The expression of FUL1, FUL2 and MBP20 is strongly upregulated during the transition from shoot apical meristem (SAM) to inflorescence-and floral meristem (IM and FM) (Park et al, 2012), suggesting that these genes may function in inflorescence meristem development like their Arabidopsis homolog.…”

Section: Introductionmentioning

confidence: 93%

“…Our screen showed that the SlFUL proteins could interact with nine other tomato MADS-domain proteins, and we observed clear differences between the interaction profiles of FUL1, FUL2, MBP10 and MBP20. All FUL-like proteins interacted with JOINTLESS (J), J2 (or SlMBP21, hereafter called J2), the fruit ripening regulator MADS-RIN, and TOMATO MADS 3 (TM3), the ortholog of the Arabidopsis flowering integrator SOC1 (Alonge et al, 2020). FUL2 exhibits the most extensive interaction network, interacting with nine proteins.…”

Section: Expression Patterns and Protein-protein Interaction Profilesmentioning

confidence: 99%

“…The MADS-box proteins J, J2, EJ2 and TM3 can form heterodimers with the FUL-like proteins, and have been shown to regulate different aspects of flowering (Szymkowiak and Irish, 2006;Thouet et al, 2012;Yuste-Lisbona et al, 2016;Soyk et al, 2019;Alonge et al, 2020). MC, which does not interact with the FULs in a yeast two-hybrid assay, but is a member of the FUL/AP1-clade, displays flowering phenotypes as well (Yuste-Lisbona et al, 2016).…”

Section: Complex Interactions Between Different Mads-domain Proteinsmentioning

confidence: 99%

“…suggesting that a complex of J and FUL2/MBP20/MC is responsible for the induction of the transition to flowering in the vegetative meristem. (S)TM3 may also be part of this complex, as lack of both TM3 and STM3 causes a mild delay in flowering (Alonge et al, 2020). In addition to delayed flowering, mc and j mutants both exhibit inflorescences that revert to vegetative growth after the formation of several flowers (Szymkowiak and Irish, 2006;Thouet et al, 2012).…”

Section: Complex Interactions Between Different Mads-domain Proteinsmentioning

confidence: 99%

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FRUITFULL-like genes regulate flowering time and inflorescence architecture in tomato

Jiang

Lubini

Hernandes‐Lopes

et al. 2020

Preprint

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The timing of flowering and inflorescence architecture are critical for the reproductive success of tomato, but the gene regulatory networks underlying these traits are still hardly explored. Here we show that the tomato FRUITFULL-like (FUL-like) genes FUL2 and MADS-BOX PROTEIN 20 (MBP20) induce flowering and repress inflorescence branching. FUL1 fulfils a less prominent role and appears to depend on FUL2 and MBP20 for its upregulation in the inflorescence meristem. Our results demonstrate that MBP10, the fourth tomato FUL-like gene, has probably lost its function. The tomato FUL-like proteins cannot homodimerize, but heterodimerize with JOINTLESS (J), SlMBP21 (J2), ENHANCER OF JOINTLESS (EJ2/MADS1) and the SOC1-homolog TOMATO MADS-box gene 3 (TM3), which are co-expressed during inflorescence meristem maturation. Transcriptome analysis revealed various interesting downstream targets, including five repressors of cytokinin signaling, which are all upregulated during the vegetative-to-reproductive transition in ful1/ful2/mbp10/mbp20 mutants. FUL2 and MBP20 can also bind in vitro to the upstream regions of these genes, thereby probably directly stimulating cell division in the meristem upon the transition to flowering. Our research reveals that the four tomato FUL-like genes have diverged functions, but together regulate the important developmental processes flowering time, inflorescence architecture and fruit development.

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MYB Genes Involved in Domestication and Crop Improvement

Albert

Allan

2021

Annual Plant Reviews Online

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Domestication of the world's crop species has been achieved through improvements in yield, and product qualities, with or without the guidance of scientific knowledge. These selection pressures are applied by breeders (and before them, farmers) both intentionally and unintentionally to improve crop features, which have often been grouped into ‘production traits’ and ‘quality traits’. New approaches to breeding that incorporate genome sequencing, mapping, and identification of genes underlying traits have revealed new variants in the family of transcription factors (TFs) called MYBs as driving important features in both these categories of domestication traits. In this article, we review the progress in understanding the role of MYB TFs in crop performance, as well as reasons to predict further gains in yield and quality centred on the MYB TF family.

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Major Impacts of Widespread Structural Variation on Gene Expression and Crop Improvement in Tomato

Cited by 597 publications

References 99 publications

SVCollector: Optimized sample selection for cost-efficient long-read population sequencing

SVCollector: Optimized sample selection for cost-efficient long-read population sequencing

FRUITFULL-like genes regulate flowering time and inflorescence architecture in tomato

MYB Genes Involved in Domestication and Crop Improvement

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