Mutations in EID1 and LNK2 caused light-conditional clock deceleration during tomato domestication

Abstract

Circadian period and phase of cultivated tomato () were changed during domestication, likely adapting the species to its new agricultural environments. Whereas the delayed circadian phase is mainly caused by allelic variation of , the genetic basis of the long circadian period has remained elusive. Here we show that a partial deletion of the clock gene is responsible for the period lengthening in cultivated tomatoes. We use resequencing data to phylogenetically classify hundreds of tomato accessions and investigate the evolution of the and mutations along successive domestication steps. We reveal signatures of selection across the genomic region of and different patterns of fixation of the mutant alleles. Strikingly, and are both involved in light input to the circadian clock, indicating that domestication specifically targeted this input pathway. In line with this, we show that the clock deceleration in the cultivated tomato is light-dependent and requires the phytochrome B1 photoreceptor. Such conditional variation in circadian rhythms may be key for latitudinal adaptation in a variety of species, including crop plants and livestock.

Molecular and transcriptional structure of the petal and leaf circadian clock inPetunia hybrida

“…The evolution of the plant circadian clock is considered an important driver of adaptation in a variety of plants including tomato, Opuntia ficus-indica or barley (Mallona et al , 2011 a ; Zakhrabekova et al , 2012; Müller et al , 2016; Müller et al , 2018). The plant clock is an important coordinator of primary and secondary metabolism in plants.…”

Genome of Solanum pimpinellifolium provides insights into structural variants during tomato breeding

“…7), suggesting that these indels may contribute to the differences in disease resistance and fruit quality traits between the wild and cultivated tomatoes. We detected several SVs known to underlie tomato domestication traits, such as the 1.4-kb deletion and 22-bp insertion in the CSR gene leading to increased fruit weight (Mu et al, 2017), the 7-kb deletion in the LNK2 gene responsible for the circadian period lengthening in cultivated tomatoes (Muller et al, 2018), the 4-kb substitution in the promoter of the TomLoxC gene, which contributes to fruit flavor (Chen et al, 2004;Shen et al, 2014;Gao et al, 2019), and the 85-bp deletion in the promoter of the ENO gene, which regulates floral meristem activity (Yuste-Lisbona et al, 2020) (Supplementary Table 7).…”

“…Genomic structural variants (SVs), including insertions/deletions (indels), inversions and duplications, are the causative genetic variants for many domestication traits of crops (Gaut et al, 2018). Empirical cases in tomato include a ~294-kb inversion at the fas locus leading to enlarged fruits (Xu et al, 2015), a 1.4-kb deletion in the CSR gene resulting in an increased fruit weight (Mu et al, 2017), a partial deletion of the LNK2 gene leading to the circadian period lengthening in cultivated tomatoes (Muller et al, 2018), and a tandem duplication at sb3 that suppresses the excessive inflorescence branching . Whole-genome SNP data have been employed to reveal the impact of human selection on the tomato genome (Lin et al, 2014) and reconstruct tomato domestication history (Razifard et al, 2020).…”

Expansion of the circadian transcriptome in Brassica rapa and genome-wide diversification of paralog expression patterns

“…As a consequence, circadian rhythms and thus much of plant biology are likely to be influenced by climate change. Examples of natural variation in plant circadian function are accumulating, as is evidence that many domestication traits that facilitated the geographic expansion of crops are due to alterations in circadian clock genes (11)(12)(13). This supports the utility in targeting circadian clock processes as a means of trait improvement without disrupting critical pathways required for growth and yield.…”