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Plant mitochondrial genomes are usually assembled and displayed as circular maps based on the widely-held view across the broad community of life scientists that circular genome-sized molecules are the primary form of plant mitochondrial DNA, despite the understanding by plant mitochondrial researchers that this is an inaccurate and outdated concept. Many plant mitochondrial genomes have one or more pairs of large repeats that can act as sites for inter- or intramolecular recombination, leading to multiple alternative arrangements (isoforms). Most mitochondrial genomes have been assembled using methods unable to capture the complete spectrum of isoforms within a species, leading to an incomplete inference of their structure and recombinational activity. To document and investigate underlying reasons for structural diversity in plant mitochondrial DNA, we used long-read (PacBio) and short-read (Illumina) sequencing data to assemble and compare mitochondrial genomes of domesticated (Lactuca sativa) and wild (L. saligna and L. serriola) lettuce species. We characterized a comprehensive, complex set of isoforms within each species and compared genome structures between species. Physical analysis of L. sativa mtDNA molecules by fluorescence microscopy revealed a variety of linear, branched, and circular structures. The mitochondrial genomes for L. sativa and L. serriola were identical in sequence and arrangement and differed substantially from L. saligna, indicating that the mitochondrial genome structure did not change during domestication. From the isoforms in our data, we infer that recombination occurs at repeats of all sizes at variable frequencies. The differences in genome structure between L. saligna and the two other Lactuca species can be largely explained by rare recombination events that rearranged the structure. Our data demonstrate that representations of plant mitochondrial genomes as simple, circular molecules are not accurate descriptions of their true nature and that in reality plant mitochondrial DNA is a complex, dynamic mixture of forms.

Lettuce ( Lactuca sativa ) is an important vegetable crop worldwide. Cultivated lettuce is believed to be domesticated from L. serriola ; however, its origins and domestication history remain to be elucidated. Here, we sequenced a total of 445 Lactuca accessions, including major lettuce crop types and wild relative species, and generated a comprehensive map of lettuce genome variations. In-depth analyses of population structure and demography revealed that lettuce was first domesticated near the Caucasus, which was marked by loss of seed shattering. We also identified the genetic architecture of other domestication traits and wild introgressions in major resistance clusters in the lettuce genome. This study provides valuable genomic resources for crop breeding and sheds light on the domestication history of cultivated lettuce. Whole-genome resequencing of 445 Lactuca accessions, including major lettuce crop types and wild relative species, provides a comprehensive map of lettuce genome variations and sheds light on the domestication history of cultivated lettuce.

Apomixis, the clonal formation of seeds, is a rare yet widely distributed trait in flowering plants. We have isolated the PARTHENOGENESIS ( PAR ) gene from apomictic dandelion that triggers embryo development in unfertilized egg cells. PAR encodes a K2-2 zinc finger, EAR-domain protein. Unlike the recessive sexual alleles, the dominant PAR allele is expressed in egg cells and has a miniature inverted-repeat transposable element (MITE) transposon insertion in the promoter. The MITE-containing promoter can invoke a homologous gene from sexual lettuce to complement dandelion LOSS OF PARTHENOGENESIS mutants. A similar MITE is also present in the promoter of the PAR gene in apomictic forms of hawkweed, suggesting a case of parallel evolution. Heterologous expression of dandelion PAR in lettuce egg cells induced haploid embryo-like structures in the absence of fertilization. Sexual PAR alleles are expressed in pollen, suggesting that the gene product releases a block on embryogenesis after fertilization in sexual species while in apomictic species PAR expression triggers embryogenesis in the absence of fertilization. The PARTHENOGENESIS ( PAR ) gene is identified in apomictic dandelion. A dominant allele has a MITE transposon insertion similar to that found in apomictic hawkweed. Expression of dandelion PAR in lettuce induces embryo-like structures without fertilization.

Seed germination and flowering, two critical developmental transitions in plant life cycles, are coordinately regulated by genetic and environmental factors to match plant establishment and reproduction to seasonal cues. The DELAY OF GERMINATION1 (DOG1) gene is involved in regulating seed dormancy in response to temperature and has also been associated genetically with pleiotropic flowering phenotypes across diverse Arabidopsis thaliana accessions and locations. Here we show that DOG1 can regulate seed dormancy and flowering times in lettuce (Lactuca sativa, Ls) and Arabidopsis through an influence on levels of microRNAs (miRNAs) miR156 and miR172. In lettuce, suppression of LsDOG1 expression enabled seed germination at high temperature and promoted early flowering in association with reduced miR156 and increased miR172 levels. In Arabidopsis, higher miR156 levels resulting from overexpression of the MIR156 gene enhanced seed dormancy and delayed flowering. These phenotypic effects, as well as conversion of MIR156 transcripts to miR156, were compromised in DOG1 loss-of-function mutant plants, especially in seeds. Overexpression of MIR172 reduced seed dormancy and promoted early flowering in Arabidopsis, and the effect on flowering required functional DOG1. Transcript levels of several genes associated with miRNA processing were consistently lower in dry seeds of Arabidopsis and lettuce when DOG1 was mutated or its expression was reduced; in contrast, transcript levels of these geneswere elevated in a DOG1 gain-of-function mutant. Our results reveal a previously unknown linkage between two critical developmental phase transitions in the plant life cycle through a DOG1–miR156–miR172 interaction.

Background Lettuce ( Lactuca sativa L. ) is an economically important vegetable crop worldwide. Lettuce is believed to be domesticated from a single wild ancestor Lactuca serriola and subsequently diverged into two major morphologically distinct vegetable types: leafy lettuce and stem lettuce. However, the role of epigenetic variation in lettuce domestication and divergence remains largely unknown. Results To understand the genetic and epigenetic basis underlying lettuce domestication and divergence, we generate single-base resolution DNA methylomes from 52 Lactuca accessions, including major lettuce cultivars and wild relatives. We find a significant increase of DNA methylation during lettuce domestication and uncover abundant epigenetic variations associated with lettuce domestication and divergence. Interestingly, DNA methylation variations specifically associated with leafy and stem lettuce are related to regulation and metabolic processes, respectively, while those associated with both types are enriched in stress responses. Moreover, we reveal that domestication-induced DNA methylation changes could influence expression levels of nearby and distal genes possibly through affecting chromatin accessibility and chromatin loop. Conclusion Our study provides population epigenomic insights into crop domestication and divergence and valuable resources for further domestication for diversity and epigenetic breeding to boost crop improvement.

Background Breeding of lettuce ( Lactuca sativa L.), the most important leafy vegetable worldwide, for enhanced disease resistance and resilience relies on multiple wild relatives to provide the necessary genetic diversity. In this study, we constructed a super-pangenome based on four Lactuca species (representing the primary, secondary and tertiary gene pools) and comprising 474 accessions. We include 68 newly sequenced accessions to improve cultivar coverage and add important foundational breeding lines. Results With the super-pangenome we find substantial presence/absence variation (PAV) and copy-number variation (CNV). Functional enrichment analyses of core and variable genes show that transcriptional regulators are conserved whereas disease resistance genes are variable. PAV-genome-wide association studies (GWAS) and CNV-GWAS are largely congruent with single-nucleotide polymorphism (SNP)-GWAS. Importantly, they also identify several major novel quantitative trait loci (QTL) for resistance against Bremia lactucae in variable regions not present in the reference lettuce genome. The usability of the super-pangenome is demonstrated by identifying the likely origin of non-reference resistance loci from the wild relatives Lactuca serriola , Lactuca saligna and Lactuca virosa . Conclusions The super-pangenome offers a broader view on the gene repertoire of lettuce, revealing relevant loci that are not in the reference genome(s). The provided methodology and data provide a strong basis for research into PAVs, CNVs and other variation underlying important biological traits of lettuce and other crops.

Leafy head is a unique type of plant architecture found in some vegetable crops,with leaves bending inward to form a compact head. The genetic and molecular mechanisms underlying leafy head in vegetables remain poorly understood. We genetically fine-mapped and cloned a major quantitative trait locus controlling heading in lettuce. The candidate gene (LsKN1) is a homolog of knotted 1 (KN1) from Zea mays. Complementation and CRISPR/Cas9 knockout experiments confirmed the role of LsKN1 in heading. In heading lettuce, there is a CACTA-like transposon inserted into the first exon of LsKN1 (LsKN1▽). The transposon sequences act as a promoter rather than an enhancer and drive high expression of LsKN1▽. The enhanced expression of LsKN1▽ is necessary but not sufficient for heading in lettuce. Data from ChIP-sequencing, electrophoretic mobility shift assays, and dual luciferase assays indicate that the LsKN1▽ protein binds the promoter of LsAS1 and down-regulates its expression to alter leaf dorsoventrality. This study provides insight into plant leaf development and will be useful for studies on heading in other vegetable crops.

Runs of homozygosity (ROH) have been extensively investigated to uncover the genomic inbred regions that reflect past population and breeding histories. In this study, we have explored the distribution and number of ROH in different Lactuca species including the cultivated lettuce varieties and their wild relatives. Next generation sequencing (NGS) technology provides the unique opportunity to study the genomes with resolution up to per-base-pair and we could compute ROH in the highest accuracy using NGS data. Our study reveals that Lactuca sativa has the longest average ROH length and fewest number of ROHs, while wild species show shorter, more numerous ROHs as expected. We found that these cultivated varieties exhibit relatively stable number of ROH and ROH lengths, with the largest median ROH count observed in Oilseed and the largest average ROH length in Crisphead. There is a significant proportion of medium-length ROHs (100 kb-1 Mb) enriched in L. sativa and L. serriola , with the highest number observed in L. serriola , while L. saligna has more short ROHs (< 10 KB), and the highest number of ROHs in the 10 KB-100 KB range were observed in Butterhead, with Stalk and Oilseed showing fewer and shorter ROHs overall. It suggests that Stalk and Oilseed were still in a process of breeding. The comparison between PLINK computation and our developed in-house algorithm shows that PLINK tends to detect longer ROH, whereas our algorithm adopts a more conservative approach, resulting in fewer and shorter ROH segments detected with higher precision more suitable for NGS data. We further analyze the distribution of ROH hotspots with a higher frequency occurred across cultivated species genomes, which has identified key genes such as DREB2B, NHL12, RPV1, and EIX2 , which play crucial roles in plant stress tolerance and immune responses, enhancing adaptability to extreme environments and providing resistance to various diseases. These findings provide fresh scientific insights into lettuce breeding, germplasm conservation, and sustainable production, highlighting the importance of understanding and managing genetic diversity in global agricultural practices.

Lettuce ( Lactuca sativa var. ramosa Hort) is an important leaf vegetable that widely cultivates due to its high-quality, short growth cycle, and less diseases. L. sativa var. ramosa Hort belongs to Asteraceae family and its evolutionary relationships with related species of Asteraceae are not completely assessed based on genome sequences. Here, we assembled the whole mitochondrial (mt) genome of L. sativa var. ramosa Hort, and performed a comparative with other related species. The L. sativa var. ramosa Hort mt genome has a typical circular structure with a length of 363,324 bp, within GC content accounted for 45.35%. In total of 71 genes, comprising 35 protein-coding genes (PCGs), 6 rRNAs, 28 tRNAs, and 2 pseudogenes were annotated. Codon preference, RNA-editing sites, repetitive sequences, and genes migrating from chloroplast (cp) to mt genomes were investigated in the L. sativa var. ramosa Hort mt genome. Nucleotide diversity (Pi) showed that the L. sativa var. ramosa Hort mt genome was relatively conserved. A Bayesian phylogenetic tree showed that L. sativa var. ramosa Hort was closely to L. sativa var . capitata and L. virosa , which belonged to the Lactuca genus in the Asteraceae family. Our findings will provide useful information to explore genetic variation, genetic diversity, and molecular breeding on the Lactuca genus.

Plant biostimulants are widely applied in agriculture for their ability to improve plant fitness. In the present work, the impact of Graminaceae -derived protein hydrolysate (P) and its lighter molecular fraction F3 (< 1 kDa) on lettuce plants, subjected to either no salt or high salt conditions, was investigated through the combination of metabolomics and transcriptomics. The results showed that both treatments significantly modulated the transcriptome and metabolome of plants under salinity stress, highlighting an induction of the hormonal response. Nevertheless, P and F3 also displayed several peculiarities. F3 specifically modulated the response to ethylene and MAPK signaling pathway, whereas P treatment induced a down-accumulation of secondary metabolites, albeit genes controlling the biosynthesis of osmoprotectants and antioxidants were up-regulated. Moreover, according with the auxin response modulation, P promoted cell wall biogenesis and plasticity in salt-stressed plants. Notably, our data also outlined an epigenetic control of gene expression induced by P treatment. Contrarily, experimental data are just partially in agreement when not stressed plants, treated with P or F3, were considered. Indeed, the reduced accumulation of secondary metabolites and the analyses of hormone pathways modulation would suggest a preferential allocation of resources towards growth, that is not coherent with the down-regulation of the photosynthetic machinery, the CO 2 assimilation rate and leaves biomass. In conclusion, our data demonstrate that, although they might activate different mechanisms, both the P and F3 can result in similar benefits, as far as the accumulation of protective osmolytes and the enhanced tolerance to oxidative stress are concerned. Notably, the F3 fraction exhibits slightly greater growth promotion effects under high salt conditions. Most importantly, this research further corroborates that biostimulants’ mode of action is dependent on plants’ physiological status and their composition, underscoring the importance of investigating the bioactivity of the different molecular components to design tailored applications for the agricultural practice.