Search

SummaryCommercial tomato (Solanum lycopersicum) is one of the most widely grown vegetable crops worldwide. Heirloom tomatoes retain extensive genetic diversity and a considerable range of fruit quality and leaf morphological traits.Here the role of leaf morphology was investigated for its impact on fruit quality. Heirloom cultivars were grown in field conditions and BRIX by Yield (BY) and other traits measured over a fourteen-week period. The complex relationships among these morphological and physiological traits were evaluated using PLS-Path Modeling, and a consensus model developed.Photosynthesis contributed strongly to vegetative biomass and sugar content of fruits but had a negative impact on yield. Conversely leaf shape, specifically rounder leaves, had a strong positive impact on both fruit sugar content and yield. Cultivars such as Stupice and Glacier, with very round leaves, had the highest performance in both fruit sugar and yield. Our model accurately predicted BY for two commercial cultivars using leaf shape data as input.This study revealed the importance of leaf shape to fruit quality in tomato, with rounder leaves having significantly improved fruit quality. This correlation was maintained across a range of diverse genetic backgrounds and shows the importance of leaf morphology in tomato crop improvement.

Parasitic weeds cause billions of dollars in agricultural losses each year worldwide.

Tomatobipinnate(bip) is a classic leaf mutant, with highly increased leaf complexity resulting from the loss of function of aBEL-LIKE HOMEODAMAIN(BELL) gene. Here, we analyzed severalbipmutants and their isogenic wildtype backgrounds for a suite of leaf morphology traits, ranging from leaf complexity, leaflet shape and size, to leaf vascular density to investigate how changes in leaf morphology influence fruit traits. Our analyses showed an unexpected relationship between leaf vein density and fruit sugar levels, where leaf vein density was negatively correlated with fruit BRIX. RNA-Seq analysis suggested variation inGlucose-6-phosphate translocator2(GPT2) gene expression caused correlated changes in leaf vein density and BRIX whenbipmutant and wildtype were compared, suggesting that the correlation between leaf vein density and fruit sugar may result from the genes regulating leaf vein development that are also involved in regulating leaf sugar biosynthesis. Our results provide a resource for further exploration of the genetic basis for the complex relationship between fruit quality and leaf traits in natural populations.

Domesticated plants and animals display tremendous diversity in various phenotypic traits and often this diversity is seen within the same species. Tomato (Solanum lycopersicum; Solanaceae) cultivars show wide variation in leaf morphology, but the influence of breeding efforts in sculpting this diversity is not known. Here, we demonstrate that a single nucleotide deletion in the homeobox motif ofBIPINNATA, which is aBEL-LIKE HOMEODOMAINgene, led to a highly complex leaf phenotype in an heirloom tomato, Silvery Fir Tree (SiFT). Additionally, a comparative gene network analysis revealed that reduced expression of the ortholog ofWUSCHEL RELATED HOMEOBOX 1is also important for the narrow leaflet phenotype seen in SiFT. Phylogenetic and comparative genome analysis using whole-genome sequencing data suggests that thebipmutation in SiFT is likely ade novomutation, instead of standing genetic variation. These results provide new insights into natural variation in phenotypic traits introduced into crops during improvement processes after domestication.

A role for programmed cell death (PCD) has been established as the basis for plant-microbe interactions. A functional plant-based cDNA library screen identified possible anti-PCD genes, including one member of the PR1 family, designated P14a, from tomato. Members of the PR1 family have been subject to extensive research in view of their possible role in resistance against pathogens. The PR1 family is represented in every plant species studied to date and homologues have been found in animals, fungi and insects. However, the biological function of the PR1 protein from plants has remained elusive in spite of extensive research regarding a role in the response of plants to disease. Constitutive expression of P14a in transgenic tomato roots protected the roots against PCD triggered by Fumonisin B1, as did the human orthologue GLIPR1, indicating a kingdom crossing function for PR1. Tobacco plants transformed with a P14a-GFP fusion construct and inoculated with Pseudomonas syringae pv. tabaci revealed that the mRNA was abundant throughout the leaves, but the fusion protein was restricted to the lesion margins, where cell death and bacterial spread were arrested. Vitus vinifera grapes expressing the PR1 homologue P14a as a transgene were protected against the cell death symptoms of Pierce's disease. A pull-down assay identified putative PR1-interacting proteins, including members of the Rac1 immune complex, known to function in innate immunity in rice and animal systems. The findings herein are consistent with a role of PR1 in the suppression of cell death-dependent disease symptoms and a possible mode of action.

Domesticated plants display diverse phenotypic traits. However, the influence of breeding effort on this phenotypic diversity remains unknown. Here, we demonstrate that a single nucleotide deletion in the homeobox motif of BIPINNATA, a BEL-LIKE HOMEODOMAIN gene, led to a highly complex leaf phenotype in an heirloom tomato (Solanum lycopersicum), Silvery Fir Tree (SiFT), which is used as a landscaping and ornamental plant. A comparative gene network analysis revealed that repression of SOLANIFOLIA, the ortholog of WUSCHEL RELATED HOMEOBOX 1, caused the narrow leaflet phenotype seen in SiFT. Comparative genomics indicated that the bip mutation in SiFT likely arose de novo and is unique to SiFT and not introgressed from other tomato genomes. These results provide new insights into the natural variation in phenotypic traits introduced into crops during improvement processes after domestication and establish homeobox genes as evolutionary hotspots.

Cuscuta species (dodders) are agriculturally destructive parasitic angiosperms. These parasitic plants use haustoria as physiological bridges to extract nutrients and water from hosts. Cuscuta campestris has a broad host range and wide geographical distribution. While some wild tomato relatives are resistant, cultivated tomatoes are generally susceptible to C. campestris infestations. However, some specific Heinz tomato hybrid cultivars exhibit resistance to dodders in the field, but their defense mechanism was unknown. Here, we discovered that the stem cortex in these resistant lines responds with local lignification upon C. campestris attachment, preventing parasite entry into the host. LIF1 (Lignin Induction Factor 1, an AP2-like transcription factor), SlMYB55, and CuRLR1 (Cuscuta R-gene for Lignin-based Resistance 1, a CC-NBS-LRR) are identified as crucial factors conferring host resistance by regulating lignification. SlWRKY16 is upregulated upon C. campestris infestation and acts as a negative regulator of LIF1 function. Intriguingly, CuRLR1 may play a role in signaling or function as a receptor for receiving Cuscuta signals or effectors to regulate lignification-based resistance. In summary, these four regulators control the lignin-based resistance response, preventing C. campestris from parasitizing these resistant tomatoes. This discovery provides a foundation for investigating multilayer resistance against Cuscuta species and has potential for application in other essential crops attacked by parasitic plants.One-sentence summaryFour key regulators confer lignin accumulation in the tomato stem cortex to block C. campestris host penetration upon infection.

Olive trees, originated from Mediterranean, have been cultivated in China for decades and show great adaption to local environment. However, research on this topic is limited. In this study, the major qualitative characteristics and changes of olive grown in southwest China were investigated. The results showed that oil accumulated during fruit development and reached its maximum value when fruit had fully ripened. Phenolic and flavonoid contents increase rapidly in the early growth stage (0-90 DAFB) and then begin to decrease as fruit ripens. Compared with olive from the Mediterranean, olive from China has special characteristics: higher moisture content in the fruit combined with lower percentages of unsaturated fatty acids and oil content. This is due to southwest China’s climate which is wetter and cooler compared to the Mediterranean. Our study suggests that southwest China’s higher annual rainfall might contribute to higher fruit moisture content while its low temperatures would be conducive to higher unsaturated fatty acid levels in the fruit.

Agrobacterium rhizogenes (or Rhizobium rhizogenes) is able to transform plant genomes and induce the production of hairy roots. We describe the use of A. rhizogenes in tomato (Solanum spp.) to rapidly assess gene expression and function. Gene expression of reporters is indistinguishable in plants transformed by Agrobacterium tumefaciens as compared with A. rhizogenes. A root cell type- and tissue-specific promoter resource has been generated for domesticated and wild tomato (Solanum lycopersicum and Solanum pennellii, respectively) using these approaches. Imaging of tomato roots using A. rhizogenes coupled with laser scanning confocal microscopy is facilitated by the use of a membrane-tagged protein fused to a red fluorescent protein marker present in binary vectors. Tomato-optimized isolation of nuclei tagged in specific cell types and translating ribosome affinity purification binary vectors were generated and used to monitor associated messenger RNA abundance or chromatin modification. Finally, transcriptional reporters, translational reporters, and clustered regularly interspaced short palindromic repeats-associated nuclease9 genome editing demonstrate that SHORT-ROOT and SCARECROW gene function is conserved between Arabidopsis (Arabidopsis thaliana) and tomato.

Parasitic flowering plants are one of the most destructive agricultural pests and have major impact on crop yields throughout the world. Being dependent on finding a host plant for growth, parasitic plants penetrate their host using specialized organs called haustoria. Haustoria establish vascular connections with the host, which enable the parasite to steal nutrients and water. The underlying molecular and developmental basis of parasitism by plants is largely unknown. In order to investigate the process of parasitism, RNAs from different stages (i.e. seed, seedling, vegetative strand, prehaustoria, haustoria, and flower) were used to de novo assemble and annotate the transcriptome of the obligate plant stem parasite dodder (Cuscuta pentagona). The assembled transcriptome was used to dissect transcriptional dynamics during dodder development and parasitism and identified key gene categories involved in the process of plant parasitism. Host plant infection is accompanied by increased expression of parasite genes underlying transport and transporter categories, response to stress and stimuli, as well as genes encoding enzymes involved in cell wall modifications. By contrast, expression of photosynthetic genes is decreased in the dodder infective stages compared with normal stem. In addition, genes relating to biosynthesis, transport, and response of phytohormones, such as auxin, gibberellins, and strigolactone, were differentially expressed in the dodder infective stages compared with stems and seedlings. This analysis sheds light on the transcriptional changes that accompany plant parasitism and will aid in identifying potential gene targets for use in controlling the infestation of crops by parasitic weeds.

Olive trees, originated from Mediterranean, have been cultivated in China for decades and show great adaption to local environment. However, research on this topic is limited. In this study, the major qualitative characteristics and changes of olive grown in southwest China were investigated. The results showed that oil accumulated during fruit development and reached its maximum value when fruit had fully ripened. Phenolic and flavonoid contents increase rapidly in the early growth stage (0–90 DAFB) and then begin to decrease as fruit ripens. Compared with olive from the Mediterranean, olive from China has special characteristics: higher moisture content in the fruit combined with lower percentages of unsaturated fatty acids and oil content. This is due to southwest China's climate which is wetter and cooler compared to the Mediterranean. Our study suggests that southwest China's higher annual rainfall might contribute to higher fruit moisture content while its low temperatures would be conducive to higher unsaturated fatty acid levels in the fruit.

Variation in gene expression, in addition to sequence polymorphisms, is known to influence developmental, physiological and metabolic traits in plants. Genetic mapping populations have facilitated identification of expression Quantitative Trait Loci (eQTL), the genetic determinants of variation in gene expression patterns. We used an introgression population developed from the wild desert-adaptedSolanum pennelliiand domesticated tomatoSolanum lycopersicumto identify the genetic basis of transcript level variation. We established the effect of each introgression on the transcriptome, and identified ~7,200 eQTL regulating the steady state transcript levels of 5,300 genes. Barnes-Hutt-distributed stochastic neighbor embedding clustering identified 42 modules revealing novel associations between transcript level patterns and biological processes. The results showed a complex genetic architecture of global transcript abundance pattern in tomato. Several genetic hotspots regulating a large number of transcript level patterns relating to diverse biological processes such as plant defense and photosynthesis were identified. Important eQTL regulating transcript level patterns were related to leaf number and complexity, and hypocotyl length. Genes associated with leaf development showed an inverse correlation with photosynthetic gene expression but eQTL regulating genes associated with leaf development and photosynthesis were dispersed across the genome. This comprehensive expression QTL analysis details the influence of these loci on plant phenotypes, and will be a valuable community resource for investigations on the genetic effects of eQTL on phenotypic traits in tomato.

Plants sense the foliar shade of competitors and alter their developmental programs through the shade-avoidance response. Internode and petiole elongation, and changes in overall leaf area and leaf mass per area, are the stereotypical architectural responses to foliar shade in the shoot. However, changes in leaf shape and complexity in response to shade remain incompletely, and qualitatively, described. Using a meta-analysis of more than 18,000 previously published leaflet outlines, we demonstrate that shade avoidance alters leaf shape in domesticated tomato (Solanum lycopersicum) and wild relatives. The effects of shade avoidance on leaf shape are subtle with respect to individual traits but are combinatorially strong. We then seek to describe the developmental origins of shade-induced changes in leaf shape by swapping plants between light treatments. Leaf size is light responsive late into development, but patterning events, such as stomatal index, are irrevocably specified earlier. Observing that shade induces increases in shoot apical meristem size, we then describe gene expression changes in early leaf primordia and the meristem using laser microdissection. We find that in leaf primordia, shade avoidance is not mediated through canonical pathways described in mature organs but rather through the expression of KNOTTED1-LIKE HOMEOBOX and other indeterminacy genes, altering known developmental pathways responsible for patterning leaf shape. We also demonstrate that shade-induced changes in leaf primordium gene expression largely do not overlap with those found in successively initiated leaf primordia, providing evidence against classic hypotheses that shaded leaf morphology results from the prolonged production of juvenile leaf types.

Leaf shape is mutable, changing in ways modulated by both development and environment within genotypes. A complete model of leaf phenotype would incorporate the changes in leaf shape during juvenile-to-adult phase transitions and the ontogeny of each leaf. Here, we provide a morphometric description of >33,000 leaflets from a set of tomato (Solanum spp) introgression lines grown under controlled environment conditions. We first compare the shape of these leaves, arising during vegetative development, with >11,000 previously published leaflets from a field setting and >11,000 leaflets from wild tomato relatives. We then quantify the changes in shape, across ontogeny, for successive leaves in the heteroblastic series. Using principal component analysis, we then separate genetic effects modulating (1) the overall shape of all leaves versus (2) the shape of specific leaves in the series, finding the former more heritable than the latter and comparing quantitative trait loci regulating each. Our results demonstrate that phenotype is highly contextual and that unbiased assessments of phenotype, for quantitative genetic or other purposes, would ideally sample the many developmental and environmental factors that modulate it.