A cytochrome P450 regulates a domestication trait in cultivated tomato

Abstract

Domestication of crop plants had effects on human lifestyle and agriculture. However, little is known about the underlying molecular mechanisms accompanying the changes in fruit appearance as a consequence of selection by early farmers. We report the fine mapping and cloning of a tomato (Solanum lycopersicum) fruit mass gene encoding the ortholog of KLUH, SlKLUH, a P450 enzyme of the CYP78A subfamily. The increase in fruit mass is predominantly the result of enlarged pericarp and septum tissues caused by increased cell number in the large fruited lines. SlKLUH also modulates plant architecture by regulating number and length of the side shoots, and ripening time, and these effects are particularly strong in plants that transgenically down-regulate SlKLUH expression carrying fruits of a dramatically reduced mass. Association mapping followed by segregation analyses revealed that a single nucleotide polymorphism in the promoter of the gene is highly associated with fruit mass. This single polymorphism may potentially underlie a regulatory mutation resulting in increased SlKLUH expression concomitant with increased fruit mass. Our findings suggest that the allele giving rise to large fruit arose in the early domesticates of tomato and becoming progressively more abundant upon further selections. We also detected association of fruit weight with CaKLUH in chile pepper (Capsicum annuum) suggesting that selection of the orthologous gene may have occurred independently in a separate domestication event. Altogether, our findings shed light on the molecular basis of fruit mass, a key domestication trait in tomato and other fruit and vegetable crops.

An InDel in the Promoter of Al-ACTIVATED MALATE TRANSPORTER9 Selected during Tomato Domestication Determines Fruit Malate Contents and Aluminum Tolerance

“…This finding is consistent with previous reports that attributed natural variation in tomato fruit size and rice grain size to expression variation in Sl-KLUH and OsSPL13, respectively (Chakrabarti et al, 2013;Si et al, 2016). Genetic complementation tests with four transgene constructs representing four haplotypes (II, III, IV, and OX) showed that the TS66 loss-of-function haplotype cannot be complemented by Sl-ALMT9 alleles from haplotype construct II, which indicates that construct II haplotypes also represent loss-of-function alleles.…”

Genome-Wide Association in Tomato Reveals 44 Candidate Loci for Fruit Metabolic Traits

“…Thus, these results open the door for subsequent analyses based on either fine localization of the putative candidate gene using a targeted resequencing approach combined with GWAS to identify and confirm the causal polymorphism or functional validation, for example by transgenic approaches to investigate the biological role of the putative candidate gene (e.g. fine-mapping of the fw3.2 locus; Chakrabarti et al, 2013).…”

“…Over the last two decades, numerous QTLs have been identified for traits such as fresh weight using linkage approaches (Frary et al, 2000;Zhang et al, 2012;Chakrabarti et al, 2013) but also for other fruit-related traits such as fruit ascorbic acid levels (Stevens et al, 2007), sensory and instrumental quality traits (Causse et al, 2002), sugar and organic acids (Fulton et al, 2002), and metabolic components (Schauer et al, 2008). Large tomato germplasm collections have been characterized at the molecular level using simple sequence repeat (Ranc et al, 2008) and single-nucleotide polymorphism (SNP) markers (Blanca et al, 2012;Shirasawa et al, 2013), giving insights into population structure, tomato evolutionary history, and the genetic architecture of traits of agronomic interest.…”

The Birth of a Black Rice Gene and Its Local Spread by Introgression

“…Furthermore, the 11.0-kb insertion, which probably occurred after the ectopic recombination event, may have led to the creation of the functional black rice promoter of Kala4 (Figure 3). Several functional polymorphisms that cause regulatory alterations have been reported to produce domestication traits (Konishi et al, 2006;Studer et al, 2011;Meyer and Purugganan, 2013;Chakrabarti et al, 2013;Xu et al, 2015). In the case of teosinte branched 1 in maize, an insertion of a transposon called Hopscotch acts as an enhancer of gene expression and contributed to the change in apical dominance of maize upon domestication (Studer et al, 2011).…”