The degree of stigma exsertion has a major influence on self-pollination efficiency in tomato, and its improvement is essential for raising productivity and for fixing advantageous traits in cultivated tomato. To study the evolution of stigma exsertion degree in tomato, we searched for genes associated with this trait and other aspects of flower morphology, including the lengths of anthers, styles, and ovaries. We performed a genome-wide association on 277 tomato accessions and discovered a novel stigma exsertion gene (SE3.1). We reannotated the structure of the gene, which encodes a C2H2-type zinc finger transcription factor. A mutation of the lead SNP creates a premature termination codon in SE3.1 and an inserted stigma in cultivated tomatoes. SE3.1 is essential for the conversion of flush stigmas to inserted stigmas. This conversion has a major impact on the rate of self-fertilization. Intriguingly, we found that both SE3.1 and Style2.1 contribute to the transition from stigma exsertion to insertion during the domestication and improvement of tomato. Style2.1 controls the first step of exserted stigmas to flush stigmas, and SE3.1 controls the second step of flush stigmas to inserted stigmas. We provide molecular details for the two-step process that controls the transition from stigma exsertion to insertion, which is of great agronomic importance in tomato.
Seed germination determines when life starts in plants, plays an important role in the efficiency of agricultural production. Nonetheless, our knowledge of the mechanisms that regulate seed germination is limited. Here, we identified a novel gene that encodes mitogen-activated protein kinase 11 (MAPK11), which the expression level in seeds of tomatoes with low germination was significantly higher than that with high germination at room temperature. Overexpression of MAPK11 in TS-9—one accession with the optimum temperature for seed germination at 25 °C—led to a decrease in seed germination, and RNA interference of MAPK11 in TS-34—one accession with the optimum temperature for seed germination at 15 °C—induced increased seed germination at room temperature. Furthermore, we found that lines overexpressing MAPK11 exhibited hypersensitivity to ABA during seed germination. These observations are at least partially explained by our finding that MAPK11 upregulates both NCED1 expression and ABA biosynthesis and that MAPK11 affects ABA signaling and negatively regulates seed germination by influencing the phosphorylation of SnRK2.2 in vivo. In addition, we found that MAPK11 may possibly inhibit SnRK1 activation by binding and phosphorylating SnRK1 in vivo. SnRK1 interacts with ABI5 and suppresses the transcription of ABI5, which contributes to ABA signaling and regulates seed germination in tomato. Thus, our findings demonstrate that in tomato, a mechanism that depends on MAPK11 phosphorylating SnRKs affects ABA signaling and ultimately influences seed germination.
The domestication of tomato has led to striking variations in fruit morphology. Here, we show a genome-wide association study (GWAS) to understand the development of the fruit tip and describe a POINTED TIP (PT) gene that encodes a C2H2-type zinc finger transcription factor. A single nucleotide polymorphism is found to change a histidine (H) to an arginine (R) in the C2H2 domain of PT and the two alleles are referred to as PTH and PTR. Knocking out PTH leads to development of pointed tip fruit. PTH functions to suppress pointed tip formation by downregulating the transcription of FRUTFULL 2 (FUL2), which alters the auxin transport. Our evolutionary analysis and previous studies by others suggest that the PTR allele likely hitch-hiked along with other selected loci during the domestication process. This study uncovers variation in PT and molecular mechanism underlying fruit tip development in tomato.
Malic acid (MA) is an important flavor acid in fruits and roles as a mediator in a series of metabolic pathways. It is important to understand the factors affecting MA metabolism for fruit flavor improvement and the cognition of MA-mediated biological processes. However, the metabolic accumulation of MA is controlled by both complex heredity and environment causing a poor prediction and regulation for MA. In this study, we carried out a genome-wide association study (GWAS) on MA using eight milestone models with two-environment repeats. A series of associated SNP variations were identified from GWAS, and 15 high-confidence annotated genes were further predicted based on the linkage disequilibrium and lead SNPs. The transcriptome data of candidate genes were explored within different tomato organs as well various fruit tissues, and suggested specific expression patterns in fruit pericarp. Based on the genetic parameters of population-differentiation and SNPs distribution, tomato MA content is more influenced by domestication sweeps while less affected by improvement sweeps in the long-term tomato breeding history. In addition, the genotype × environment interaction might contribute to the difference in domestication phenotypic data under different environments. This study provides new genetic insights into how tomato changed the MA content during breeding and made available function-based markers for marker-assisted selection breeding.
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