Publications by authors named "Richard G F Visser"

272 Publications

Dissecting the Genotypic Variation of Growth Responses to Far-Red Radiation in Tomato.

Front Plant Sci 2020 13;11:614714. Epub 2021 Jan 13.

Horticulture and Product Physiology, Department of Plant Sciences, Wageningen University & Research, Wageningen, Netherlands.

The recent development of light-emitting diodes (LEDs) and their application in modern horticulture stimulated studies demonstrating that additional far-red (FR) radiation (700-800 nm) increases plant dry mass. This effect of FR has been explained by improved photosynthesis and/or plant architecture. However, the genotypic variation in this response is largely unknown. Here, we aim to explore and explain the genotypic variation in growth responses to additional FR. We expected the genotypic variation in the responses of plant dry mass to additional FR. Further, we hypothesized that a significant improvement of both net assimilation rate (NAR) and leaf area ratio (LAR) is responsible for a strong dry mass increase under additional FR, while some genotypes respond only marginally or even negatively in NAR or LAR under FR, thus resulting in a weak FR effect on plant dry mass. To test these hypotheses, we grew 33 different tomato genotypes for 21 days with 0, 25, or 100 μmol m s of FR added to a common white + red LED background lighting of 150 μmol m s. Genotypes responded similarly with respect to plant height, stem dry mass, and shoot:root ratio; i.e., they all increased with increasing FR. However, the response of total plant dry mass varied among genotypes. We categorized the genotypes into three groups (strongly, moderately, and weakly responding groups) based on their relative response in total plant dry mass to FR. Growth component analysis revealed that the strongly responding genotypes increased strongly in NAR rather than LAR. The weakly responding genotypes, however, showed a substantial increase in LAR but not NAR. The increase in LAR was due to the increase in specific leaf area. Leaf mass fraction, which is the other component of LAR, decreased with FR and did not differ between groups. In conclusion, tomato genotypes that increased strongly in NAR in response to FR were able to achieve a more substantial increase in dry mass than did other genotypes. This is the first study to explain the differences in growth responses of a large number of tomato genotypes toward FR in their light environment.
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http://dx.doi.org/10.3389/fpls.2020.614714DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7838372PMC
January 2021

Potato CYCLING DOF FACTOR 1 and its lncRNA counterpart StFLORE link tuber development and drought response.

Plant J 2021 Feb 11;105(4):855-869. Epub 2021 Feb 11.

Plant Breeding, Wageningen University & Research, PO Box 386, Wageningen, 6700 AJ, the Netherlands.

Plants regulate their reproductive cycles under the influence of environmental cues, such as day length, temperature and water availability. In Solanum tuberosum (potato), vegetative reproduction via tuberization is known to be regulated by photoperiod, in a very similar way to flowering. The central clock output transcription factor CYCLING DOF FACTOR 1 (StCDF1) was shown to regulate tuberization. We now show that StCDF1, together with a long non-coding RNA (lncRNA) counterpart, named StFLORE, also regulates water loss through affecting stomatal growth and diurnal opening. Both natural and CRISPR-Cas9 mutations in the StFLORE transcript produce plants with increased sensitivity to water-limiting conditions. Conversely, elevated expression of StFLORE, both by the overexpression of StFLORE or by the downregulation of StCDF1, results in an increased tolerance to drought through reducing water loss. Although StFLORE appears to act as a natural antisense transcript, it is in turn regulated by the StCDF1 transcription factor. We further show that StCDF1 is a non-redundant regulator of tuberization that affects the expression of two other members of the potato StCDF gene family, as well as StCO genes, through binding to a canonical sequence motif. Taken together, we demonstrate that the StCDF1-StFLORE locus is important for vegetative reproduction and water homeostasis, both of which are important traits for potato plant breeding.
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http://dx.doi.org/10.1111/tpj.15093DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7985872PMC
February 2021

Analysis of QTL DM4.1 for Downy Mildew Resistance in Cucumber Reveals Multiple subQTL: A Novel as Candidate Gene for the Most Important subQTL.

Front Plant Sci 2020 22;11:569876. Epub 2020 Oct 22.

Plant Breeding, Wageningen University & Research, Wageningen, Netherlands.

One of the biggest problems in cucumber cultivation is cucurbit downy mildew (DM), caused by the obligate biotroph . Whereas DM in cucumber was previously efficiently controlled by the gene from Indian cucumber accession PI 197087, this resistance was broken by new DM strains, prompting the search for novel sources of resistance. A promising source of resistance is the wild cucumber accession PI 197088. It was previously shown that DM resistance in this genotype inherits polygenically. In this paper, we put the focus on one of the QTL, DM4.1 that is located on chromosome 4. QTL DM4.1 was shown to consist of three subQTL: DM4.1.1 affected pathogen-induced necrosis, DM4.1.2 was shown to have an additive effect on sporulation, and DM4.1.3 had a recessive effect on chlorosis as well as an effect on sporulation. Near-isogenic lines (NILs) were produced by introgressing the subQTLs into a susceptible cucumber line (HS279) with good horticultural traits. Transcriptomic analysis revealed that many genes in general, and defense pathway genes in particular, were differentially expressed in NIL DM4.1.1/.2 compared to NIL DM4.1.3 and the susceptible parent HS279. This indicates that the resistance from subQTL DM4.1.1 and/or subQTL DM4.1.2 likely involves defense signaling pathways, whereas resistance due to subQTL DM4.1.3 is more likely to be independent of known defense pathways. Based on fine-mapping data, we identified the gene as a likely candidate for subQTL DM4.1.2, as this gene was found to have a loss-of-function mutation in the susceptible parent HS279, and was strongly upregulated by inoculation in NIL DM4.1.1/.2. Heterologous expression of this gene triggered necrosis, providing further evidence that this gene is indeed causal for subQTL DM4.1.2.
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http://dx.doi.org/10.3389/fpls.2020.569876DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7649820PMC
October 2020

Exploration of a Resequenced Tomato Core Collection for Phenotypic and Genotypic Variation in Plant Growth and Fruit Quality Traits.

Genes (Basel) 2020 Oct 29;11(11). Epub 2020 Oct 29.

Plant Breeding, Wageningen University & Research, P.O. Box 386, 6700 AJ Wageningen, The Netherlands.

A tomato core collection consisting of 122 gene bank accessions, including landraces, old cultivars, and wild relatives, was explored for variation in several plant growth, yield and fruit quality traits. The resequenced accessions were also genotyped with respect to a number of mutations or variations in key genes known to underlie these traits. The yield-related traits fruit number and fruit weight were much higher in cultivated varieties when compared to wild accessions, while, in wild tomato accessions, Brix was higher than in cultivated varieties. Known mutations in fruit size and shape genes could well explain the fruit size variation, and fruit colour variation could be well explained by known mutations in key genes of the carotenoid and flavonoid pathway. The presence and phenotype of several plant architecture affecting mutations, such as (), ( (), and () were also confirmed. This study provides valuable phenotypic information on important plant growth- and quality-related traits in this collection. The allelic distribution of known genes that underlie these traits provides insight into the role and importance of these genes in tomato domestication and breeding. This resource can be used to support (precision) breeding strategies for tomato crop improvement.
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http://dx.doi.org/10.3390/genes11111278DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7692805PMC
October 2020

The NLR Protein Encoded by the Resistance Gene Is Triggered by the Replication-Associated Protein Rep/C1 of Tomato Yellow Leaf Curl Virus.

Front Plant Sci 2020 10;11:545306. Epub 2020 Sep 10.

Plant Breeding, Wageningen University & Research, Wageningen, Netherlands.

The whitefly-transmitted tomato yellow leaf curl virus (TYLCV) is one of the most destructive viral pathogens of cultivated tomato. To combat TYLCV, resistance gene has been introduced into cultivated tomato () from wild tomato species by interspecific crossing. Introgression lines with contain a large inversion compared with , which causes severe suppression of recombination and has hampered the cloning of so far. Here, we report the fine-mapping and cloning of using crosses between a introgression line and several susceptible accessions. was shown to encode a nucleotide-binding leucine-rich repeat (NLR) protein. For breeding purposes, a highly specific DNA marker tightly linked to the gene was developed permitting marker-assisted selection. The resistance mediated by was effective against the Israel strain of TYLCV (TYLCV-IL) and tomato yellow leaf curl virus-[China : Shanghai2] (TYLCV-[CN : SH2]), but not against tomato yellow leaf curl Sardinia virus (TYLCSV) and leafhopper-transmitted beet curly top virus (BCTV). By co-infiltration experiments we showed that transient expression of the Rep/C1 protein of TYLCV, but not of TYLCSV triggered a hypersensitive response (HR) in plants co-expressing the gene. Our results indicate that the / gene of TYLCV-IL presents the avirulence determinant of mediated resistance.
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http://dx.doi.org/10.3389/fpls.2020.545306DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7511541PMC
September 2020

Haplotype-resolved genome analyses of a heterozygous diploid potato.

Nat Genet 2020 10 28;52(10):1018-1023. Epub 2020 Sep 28.

Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Area, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China.

Potato (Solanum tuberosum L.) is the most important tuber crop worldwide. Efforts are underway to transform the crop from a clonally propagated tetraploid into a seed-propagated, inbred-line-based hybrid, but this process requires a better understanding of potato genome. Here, we report the 1.67-Gb haplotype-resolved assembly of a diploid potato, RH89-039-16, using a combination of multiple sequencing strategies, including circular consensus sequencing. Comparison of the two haplotypes revealed ~2.1% intragenomic diversity, including 22,134 predicted deleterious mutations in 10,642 annotated genes. In 20,583 pairs of allelic genes, 16.6% and 30.8% exhibited differential expression and methylation between alleles, respectively. Deleterious mutations and differentially expressed alleles were dispersed throughout both haplotypes, complicating strategies to eradicate deleterious alleles or stack beneficial alleles via meiotic recombination. This study offers a holistic view of the genome organization of a clonally propagated diploid species and provides insights into technological evolution in resolving complex genomes.
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http://dx.doi.org/10.1038/s41588-020-0699-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7527274PMC
October 2020

A Hitchhiker's guide to the potato wart disease resistance galaxy.

Theor Appl Genet 2020 Dec 12;133(12):3419-3439. Epub 2020 Sep 12.

Plant Breeding, Wageningen University and Research, P.O. Box 386, 6700 AJ, Wageningen, The Netherlands.

Key Message: Two novel major effect loci (Sen4 and Sen5) and several minor effect QTLs for potato wart disease resistance have been mapped. The importance of minor effect loci to bring full resistance to wart disease was investigated. Using the newly identified and known wart disease resistances, a panel of potato breeding germplasm and Solanum wild species was screened. This provided a state-of-the-art "hitch-hikers-guide" of complementary wart disease resistance sources. Potato wart disease, caused by the obligate biotrophic soil-born fungus Synchytrium endobioticum, is the most important quarantine disease of potato. Because of its huge impact on yield, the lack of chemical control and the formation of resting spores with long viability, breeding for resistant varieties combined with strict quarantine measures are the only way to efficiently and durably manage the disease. In this study, we set out to make an inventory of the different resistance sources. Using a Genome-Wide Association Study (GWAS) in the potato breeding genepool, we identified Sen4, associated with pathotypes 2, 6 and 18 resistance. Associated SNPs mapped to the south arm of chromosome 12 and were validated to be linked to resistance in one full-sib population. Also, a bulked segregant analysis combined with a Comparative Subsequence Sets Analysis (CoSSA) resulted in the identification of Sen5, associated with pathotypes 2, 6 and 18 resistance, on the south arm of chromosome 5. In addition to these two major effect loci, the GWAS and CoSSA allowed the identification of several quantitative trait loci necessary to bring full resistance to certain pathotypes. Panels of varieties and Solanum accessions were screened for the presence of Sen1, Sen2, Sen3, Sen4 and Sen5. Combined with pedigree analysis, we could trace back some of these genes to the ancestral resistance donors. This analysis revealed complementary resistance sources and allows elimination of redundancy in wart resistance breeding programs.
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http://dx.doi.org/10.1007/s00122-020-03678-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7567731PMC
December 2020

Solyntus, the New Highly Contiguous Reference Genome for Potato ().

G3 (Bethesda) 2020 10 5;10(10):3489-3495. Epub 2020 Oct 5.

Plant Breeding, Wageningen University and Research, 6708 PB, Wageningen, The Netherlands

With the rapid expansion of the application of genomics and sequencing in plant breeding, there is a constant drive for better reference genomes. In potato (), the third largest food crop in the world, the related species , designated "DM", has been used as the most popular reference genome for the last 10 years. Here, we introduce the sequenced genome of Solyntus as the next standard reference in potato genome studies. A true made up of 116 contigs that is also highly homozygous, diploid, vigorous and self-compatible, Solyntus provides a more direct and contiguous reference then ever before available. It was constructed by sequencing with state-of-the-art long and short read technology and assembled with Canu. The 116 contigs were assembled into scaffolds to form each pseudochromosome, with three contigs to 17 contigs per chromosome. This assembly contains 93.7% of the single-copy gene orthologs from the Solanaceae set and has an N50 of 63.7 Mbp. The genome and related files can be found at https://www.plantbreeding.wur.nl/Solyntus/ With the release of this research line and its draft genome we anticipate many exciting developments in (diploid) potato research.
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http://dx.doi.org/10.1534/g3.120.401550DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7534448PMC
October 2020

Divergent Evolution of PcF/SCR74 Effectors in Oomycetes Is Associated with Distinct Recognition Patterns in Solanaceous Plants.

mBio 2020 06 30;11(3). Epub 2020 Jun 30.

Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands

Plants deploy cell surface receptors known as pattern-recognition receptors (PRRs) that recognize non-self molecules from pathogens and microbes to defend against invaders. PRRs typically recognize microbe-associated molecular patterns (MAMPs) that are usually widely conserved, some even across kingdoms. Here, we report an oomycete-specific family of small secreted cysteine-rich (SCR) proteins that displays divergent patterns of sequence variation in the Irish potato famine pathogen A subclass that includes the conserved effector PcF from activates immunity in a wide range of plant species. In contrast, the more diverse SCR74 subclass is specific to and tends to trigger immune responses only in a limited number of wild potato genotypes. The SCR74 response was recently mapped to a G-type lectin receptor kinase () locus in the wild potato subsp. The locus displays a high diversity in host species compared to other solanaceous plants. We propose that the diversification of the SCR74 proteins in is driven by a fast coevolutionary arms race with cell surface immune receptors in wild potato, which contrasts the presumed slower dynamics between conserved apoplastic effectors and PRRs. Understanding the molecular determinants of plant immune responses to these divergent molecular patterns in oomycetes is expected to contribute to deploying multiple layers of disease resistance in crop plants. Immune receptors at the plant cell surface can recognize invading microbes. The perceived microbial molecules are typically widely conserved and therefore the matching surface receptors can detect a broad spectrum of pathogens. Here we describe a family of small extracellular proteins that consists of conserved subfamilies that are widely recognized by solanaceous plants. Remarkably, one subclass of SCR74 proteins is highly diverse, restricted to the late blight pathogen and is specifically detected in wild potato plants. The diversification of this subfamily exhibits signatures of a coevolutionary arms race with surface receptors in potato. Insights into the molecular interaction between these potato-specific receptors and the recognized proteins are expected to contribute to disease resistance breeding in potato.
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http://dx.doi.org/10.1128/mBio.00947-20DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7327169PMC
June 2020

CRISPR/Cas9-targeted mutagenesis of the tomato susceptibility gene PMR4 for resistance against powdery mildew.

BMC Plant Biol 2020 Jun 19;20(1):284. Epub 2020 Jun 19.

Plant Breeding, Wageningen University & Research, Droevendaalsesteeg 1, 6708, PB, Wageningen, The Netherlands.

Background: The development of CRISPR/Cas9 technology has facilitated targeted mutagenesis in an efficient and precise way. Previously, RNAi silencing of the susceptibility (S) gene PowderyMildewResistance 4 (PMR4) in tomato has been shown to enhance resistance against the powdery mildew pathogen Oidium neolycopersici (On).

Results: To study whether full knock-out of the tomato PMR4 gene would result in a higher level of resistance than in the RNAi-silenced transgenic plants we generated tomato PMR4 CRISPR mutants. We used a CRISPR/Cas9 construct containing four single-guide RNAs (sgRNAs) targeting the tomato PMR4 gene to increase the possibility of large deletions in the mutants. After PCR-based selection and sequencing of transformants, we identified five different mutation events, including deletions from 4 to 900-bp, a 1-bp insertion and a 892-bp inversion. These mutants all showed reduced susceptibility to On based on visual scoring of disease symptoms and quantification of relative fungal biomass. Histological observations revealed a significantly higher occurrence of hypersensitive response-like cell death at sites of fungal infection in the pmr4 mutants compared to wild-type plants. Both haustorial formation and hyphal growth were diminished but not completely inhibited in the mutants.

Conclusion: CRISPR/Cas-9 targeted mutagenesis of the tomato PMR4 gene resulted in mutants with reduced but not complete loss of susceptibility to the PM pathogen On. Our study demonstrates the efficiency and versatility of the CRISPR/Cas9 system as a powerful tool to study and characterize S-genes by generating different types of mutations.
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http://dx.doi.org/10.1186/s12870-020-02497-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7304142PMC
June 2020

The genetic and functional analysis of flavor in commercial tomato: the FLORAL4 gene underlies a QTL for floral aroma volatiles in tomato fruit.

Plant J 2020 08 21;103(3):1189-1204. Epub 2020 Jun 21.

Plant Breeding, Wageningen University and Research, Droevendaalsesteeg 1, Wageningen, 6708PB, the Netherlands.

Tomato (Solanum lycopersicum L.) has become a popular model for genetic studies of fruit flavor in the last two decades. In this article we present a study of tomato fruit flavor, including an analysis of the genetic, metabolic and sensorial variation of a collection of contemporary commercial glasshouse tomato cultivars, followed by a validation of the associations found by quantitative trait locus (QTL) analysis of representative biparental segregating populations. This led to the identification of the major sensorial and chemical components determining fruit flavor variation and detection of the underlying QTLs. The high representation of QTL haplotypes in the breeders' germplasm suggests that there is great potential for applying these QTLs in current breeding programs aimed at improving tomato flavor. A QTL on chromosome 4 was found to affect the levels of the phenylalanine-derived volatiles (PHEVs) 2-phenylethanol, phenylacetaldehyde and 1-nitro-2-phenylethane. Fruits of near-isogenic lines contrasting for this locus and in the composition of PHEVs significantly differed in the perception of fruity and rose-hip-like aroma. The PHEV locus was fine mapped, which allowed for the identification of FLORAL4 as a candidate gene for PHEV regulation. Using a gene-editing-based (CRISPR-CAS9) reverse-genetics approach, FLORAL4 was demonstrated to be the key factor in this QTL affecting PHEV accumulation in tomato fruit.
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http://dx.doi.org/10.1111/tpj.14795DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7496274PMC
August 2020

Options to Reform the European Union Legislation on GMOs: Post-authorization and Beyond.

Trends Biotechnol 2020 05 12;38(5):465-467. Epub 2020 Feb 12.

Plant Breeding, Wageningen University & Research, PO Box 386, 6700AJ Wageningen, The Netherlands.

We discuss options to reform the EU genetically modified organism (GMO) regulatory framework, make risk assessment and decision-making more consistent with scientific principles, and lay the groundwork for international coherence. In this third of three articles, we focus on labeling and coexistence as well as discuss the political reality and potential ways forward.
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http://dx.doi.org/10.1016/j.tibtech.2019.12.015DOI Listing
May 2020

RLP/K enrichment sequencing; a novel method to identify receptor-like protein (RLP) and receptor-like kinase (RLK) genes.

New Phytol 2020 08 22;227(4):1264-1276. Epub 2020 May 22.

Plant Breeding, Wageningen University and Research, Droevendaalsesteeg 1, 6708, PB, Wageningen, the Netherlands.

The identification of immune receptors in crop plants is time-consuming but important for disease control. Previously, resistance gene enrichment sequencing (RenSeq) was developed to accelerate mapping of nucleotide-binding domain and leucine-rich repeat containing (NLR) genes. However, resistances mediated by pattern recognition receptors (PRRs) remain less utilized. Here, our pipeline shows accelerated mapping of PRRs. Effectoromics leads to precise identification of plants with target PRRs, and subsequent RLP/K enrichment sequencing (RLP/KSeq) leads to detection of informative single nucleotide polymorphisms that are linked to the trait. Using Phytophthora infestans as a model, we identified Solanum microdontum plants that recognize the apoplastic effectors INF1 or SCR74. RLP/KSeq in a segregating Solanum population confirmed the localization of the INF1 receptor on chromosome 12, and led to the rapid mapping of the response to SCR74 to chromosome 9. By using markers obtained from RLP/KSeq in conjunction with additional markers, we fine-mapped the SCR74 receptor to a 43-kbp G-LecRK locus. Our findings show that RLP/KSeq enables rapid mapping of PRRs and is especially beneficial for crop plants with large and complex genomes. This work will enable the elucidation and characterization of the nonNLR plant immune receptors and ultimately facilitate informed resistance breeding.
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http://dx.doi.org/10.1111/nph.16608DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7383770PMC
August 2020

Options to Reform the European Union Legislation on GMOs: Risk Governance.

Trends Biotechnol 2020 04 12;38(4):349-351. Epub 2020 Feb 12.

Plant Breeding, Wageningen University & Research, PO Box 386, 6700AJ Wageningen, The Netherlands.

Here, we discuss options to reform the EU genetically modified organism (GMO) regulatory framework, to make risk assessment and decision-making more consistent with scientific principles, and to lay the groundwork for international coherence. We discussed the scope and definitions in a previous article and, thus, here we focus on the procedures for risk assessment and risk management.
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http://dx.doi.org/10.1016/j.tibtech.2019.12.016DOI Listing
April 2020

Enabling reusability of plant phenomic datasets with MIAPPE 1.1.

New Phytol 2020 07 25;227(1):260-273. Epub 2020 Apr 25.

Université Paris-Saclay, INRAE, URGI, Versailles, 78026, France.

Enabling data reuse and knowledge discovery is increasingly critical in modern science, and requires an effort towards standardising data publication practices. This is particularly challenging in the plant phenotyping domain, due to its complexity and heterogeneity. We have produced the MIAPPE 1.1 release, which enhances the existing MIAPPE standard in coverage, to support perennial plants, in structure, through an explicit data model, and in clarity, through definitions and examples. We evaluated MIAPPE 1.1 by using it to express several heterogeneous phenotyping experiments in a range of different formats, to demonstrate its applicability and the interoperability between the various implementations. Furthermore, the extended coverage is demonstrated by the fact that one of the datasets could not have been described under MIAPPE 1.0. MIAPPE 1.1 marks a major step towards enabling plant phenotyping data reusability, thanks to its extended coverage, and especially the formalisation of its data model, which facilitates its implementation in different formats. Community feedback has been critical to this development, and will be a key part of ensuring adoption of the standard.
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http://dx.doi.org/10.1111/nph.16544DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7317793PMC
July 2020

Options to Reform the European Union Legislation on GMOs: Scope and Definitions.

Trends Biotechnol 2020 03 12;38(3):231-234. Epub 2020 Feb 12.

Plant Breeding, Wageningen University & Research, 6700AJ Wageningen, The Netherlands.

We discuss options to reform the EU genetically modified organisms (GMO) regulatory framework, make risk assessment and decision-making more consistent with scientific principles, and lay the groundwork for international coherence. The first in a three-part series, this article focuses on reform options related to the scope of the legislation and the GMO definition.
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http://dx.doi.org/10.1016/j.tibtech.2019.12.002DOI Listing
March 2020

Distribution of P1(D1) wart disease resistance in potato germplasm and GWAS identification of haplotype-specific SNP markers.

Theor Appl Genet 2020 Jun 11;133(6):1859-1871. Epub 2020 Feb 11.

Plant Breeding, Wageningen University and Research, Droevendaalsesteeg 1, 6708 PB, Wageningen, The Netherlands.

Key Message: A Genome-Wide Association Study using 330 commercial potato varieties identified haplotype specific SNP markers associated with pathotype 1(D1) wart disease resistance. Synchytrium endobioticum is a soilborne obligate biotrophic fungus responsible for wart disease. Growing resistant varieties is the most effective way to manage the disease. This paper addresses the challenge to apply molecular markers in potato breeding. Although markers linked to Sen1 were published before, the identification of haplotype-specific single-nucleotide polymorphisms may result in marker assays with high diagnostic value. To identify hs-SNP markers, we performed a genome-wide association study (GWAS) in a panel of 330 potato varieties representative of the commercial potato gene pool. SNP markers significantly associated with pathotype 1 resistance were identified on chromosome 11, at the position of the previously identified Sen1 locus. Haplotype specificity of the SNP markers was examined through the analysis of false positives and false negatives and validated in two independent full-sib populations. This paper illustrates why it is not always feasible to design markers without false positives and false negatives for marker-assisted selection. In the case of Sen1, founders could not be traced because of a lack of identity by descent and because of the decay of linkage disequilibrium between Sen1 and flanking SNP markers. Sen1 appeared to be the main source of pathotype 1 resistance in potato varieties, but it does not explain all the resistance observed. Recombination and introgression breeding may have introduced new, albeit rare haplotypes involved in pathotype 1 resistance. The GWAS approach, in such case, is instrumental to identify SNPs with the best possible diagnostic value for marker-assisted breeding.
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http://dx.doi.org/10.1007/s00122-020-03559-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7237394PMC
June 2020

Breeding Has Increased the Diversity of Cultivated Tomato in The Netherlands.

Front Plant Sci 2019 20;10:1606. Epub 2019 Dec 20.

Plant Breeding, Wageningen University & Research, Wageningen, Netherlands.

It is generally believed that domestication and breeding of plants has led to genetic erosion, including loss of nutritional value and resistances to diseases, especially in tomato. We studied the diversity dynamics of greenhouse tomato varieties in NW Europe, especially The Netherlands, over the last seven decades. According to the used SNP array, the genetic diversity was indeed very low during the 1960s, but is now eight times higher when compared to that dip. The pressure since the 1970s to apply less pesticides led to the introgression of many disease resistances from wild relatives, representing the first boost of genetic diversity. In Europe a second boost ensued, largely driven by German popular media who named poor tasting tomatoes (water bombs). The subsequent collapse of Dutch tomato exports to Germany fueled breeding for fruit flavor, further increasing diversity since the 1990s. The increased diversity in composition of aroma volatiles observed starting from 1990s may reflect the efforts of breeders to improve fruit quality. Specific groups of aroma compounds showed different quantitative trend over the decades studied. Our study provides compelling evidence that breeding has increased the diversity of tomato varieties considerably since the 1970s.
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http://dx.doi.org/10.3389/fpls.2019.01606DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6932954PMC
December 2019

Morphological and physiological responses of the potato stem transport tissues to dehydration stress.

Planta 2020 Jan 8;251(2):45. Epub 2020 Jan 8.

Plant Breeding, Wageningen University and Research, Droevendaalsesteeg 1, 6708 PB, Wageningen, The Netherlands.

Main Conclusion: Adaptation of the xylem under dehydration to smaller sized vessels and the increase in xylem density per stem area facilitate water transport during water-limiting conditions, and this has implications for assimilate transport during drought. The potato stem is the communication and transport channel between the assimilate-exporting source leaves and the terminal sink tissues of the plant. During environmental stress conditions like water scarcity, which adversely affect the performance (canopy growth and tuber yield) of the potato plant, the response of stem tissues is essential, however, still understudied. In this study, we investigated the response of the stem tissues of cultivated potato grown in the greenhouse to dehydration using a multidisciplinary approach including physiological, biochemical, morphological, microscopic, and magnetic resonance imaging techniques. We observed the most significant effects of water limitation in the lower stem regions of plants. The light microscopy analysis of the potato stem sections revealed that plants exposed to this particular dehydration stress have higher total xylem density per unit area than control plants. This increase in the total xylem density was accompanied by an increase in the number of narrow-diameter xylem vessels and a decrease in the number of large-diameter xylem vessels. Our MRI approach revealed a diurnal rhythm of xylem flux between day and night, with a reduction in xylem flux that is linked to dehydration sensitivity. We also observed that sink strength was the main driver of assimilate transport through the stem in our data set. These findings may present potential breeding targets for drought tolerance in potato.
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http://dx.doi.org/10.1007/s00425-019-03336-7DOI Listing
January 2020

The ability to manipulate ROS metabolism in pepper may affect aphid virulence.

Hortic Res 2020 1;7. Epub 2020 Jan 1.

Plant Breeding, Wageningen University & Research, P.O. Box 386, 6700 AJ Wageningen, Netherlands.

has severe economic impact on pepper () cultivation. Previously, we identified two populations of , NL and SW, that were avirulent and virulent, respectively on accession PB2013071. The transcriptomics approach used in the current study, which is the first study to explore the pepper-aphid interaction at the whole genome gene expression level, revealed genes whose expression is differentially regulated in pepper accession PB2013071 upon infestation with these populations. The NL population induced ROS production genes, while the SW population induced ROS scavenging genes and repressed ROS production genes. We also found that the SW population can induce the removal of ROS which accumulated in response to preinfestion with the NL population, and that preinfestation with the SW population significantly improved the performance of the NL population. This paper supports the hypothesis that can overcome the resistance in accession PB2013071 probably because of its ability to manipulate plant defense response especially the ROS metabolism and such ability may benefit avirulent conspecific aphids.
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http://dx.doi.org/10.1038/s41438-019-0231-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6938493PMC
January 2020

Carbon partitioning mechanisms in POTATO under drought stress.

Plant Physiol Biochem 2020 Jan 12;146:211-219. Epub 2019 Nov 12.

Plant Breeding, Wageningen University & Research, Droevendaalsesteeg 1, 6708 PB, Wageningen, The Netherlands. Electronic address:

Potato (Solanum tuberosum) is an important food crop consumed all over the world, but it is generally sensitive to drought conditions. One of the major physiological processes affected by drought stress is carbon partitioning: the plant's choice of where to allocate its photoassimilates. Our aim was to investigate the molecular factors and possible bottlenecks affecting carbon partitioning during drought. We studied potato cultivars with contrasting drought responses in the greenhouse in the years 2013-2015, and further investigated the expression of genes involved in carbon partitioning and metabolite levels. Our results indicate that one of the most severe effects of drought stress on potato is the arrest of stolon differentiation and formation of tubers. We also identified some physiological traits like stomatal conductance and chlorophyll content as affecting carbon assimilation, partitioning and eventual tuber yield. The gene expressions and biochemical analyses highlight the various tissues prioritized by the plant for assimilate transport during drought stress, and give indications of what distinguishes drought tolerance and sensitivity of cultivated potato. Some of the key genes studied (like Sucrose synthase and Sucrose transporters) may be inclusive breeding targets for drought tolerance in potato.
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http://dx.doi.org/10.1016/j.plaphy.2019.11.019DOI Listing
January 2020

High-Altitude Wild Species LA385-A Potential Source for Improvement of Plant Growth and Photosynthetic Performance at Suboptimal Temperatures.

Front Plant Sci 2019 24;10:1163. Epub 2019 Sep 24.

Plant Breeding, Wageningen University and Research, Wageningen, Netherlands.

Plant growth, development, and yield of current tomato cultivars are directly affected by low temperatures. Although wild tomato species have been suggested as a potential source for low temperature tolerance, very little is known about their behavior during the reproductive phase. Here, we investigated the impact of suboptimal temperatures (SOT, 16/14°C), as compared to control temperatures (CT, 22/20°C), on plant growth, photosynthetic capacity, and carbohydrate metabolism. Under these conditions, two genotypes were analyzed: a cultivar Moneymaker and a high-altitude wild species LA385, from flowering onset until a later stage of fruit development. Total dry matter production in cv. Moneymaker was reduced up to 30% at SOT, whereas it was hardly affected in wild accession LA385. Specific leaf area, total leaf area, and number of fruits were also decreased at SOT in cv. Moneymaker. In contrast, wild accession LA385 showed an acclimation to SOT, in which Φ and net CO assimilation rates were less affected; a similar specific leaf area; higher total leaf area; and higher number of fruits compared to those at CT. In addition, LA385 appeared to have a more distinct sucrose metabolism than cv. Moneymaker at both temperatures, in which it had higher contents of sucrose-6-phosphate, sucrose, and ratio of sucrose: starch in leaves and higher ratio of sucrose: hexose in fruits. Overall, our findings indicate that wild accession LA385 is able to acclimate well to SOT during the reproductive phase, whereas growth and development of cv. Moneymaker is reduced at SOT.
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http://dx.doi.org/10.3389/fpls.2019.01163DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6769098PMC
September 2019

Aphid resistance in Capsicum maps to a locus containing LRR-RLK gene analogues.

Theor Appl Genet 2020 Jan 8;133(1):227-237. Epub 2019 Oct 8.

Plant Breeding, Wageningen University and Research, P.O. Box 386, 6700 AJ, Wageningen, The Netherlands.

Key Message: A QTL for aphid resistance on pepper chromosome 2 was identified and validated. This QTL affects aphid survival and reproduction, and was fine mapped to a locus containing LRR-RLK analogues. Myzus persicae is one of the most threatening insect pests that adversely affects pepper (Capsicum) cultivation. Resistance to aphids was previously identified in Capsicum baccatum. This study aimed at elucidating the genetics of aphid resistance in C. baccatum. A QTL analysis was carried out for M. persicae resistance in an F population derived from an intraspecific cross between a highly resistant plant and a susceptible plant. Survival and reproduction were used as resistance parameters. Interval mapping detected two QTLs affecting aphid survival (Rmpas-1) and reproduction (Rmprp-1), respectively, both localized in the same area and sharing the same top marker on chromosome 2. Use of this marker as co-factor in multiple-QTL mapping analysis revealed a second, minor QTL (Rmprp-2) only affecting aphid reproduction, on chromosome 4. Fine mapping confirmed the effects of Rmpas-1 and Rmprp-1 and narrowed the major QTL Rmprp-1 down to a genomic region of 96 kb which is predicted to encode four analogues of resistance genes of the receptor-like kinase family containing a leucine-rich repeat domain (LRR-RLKs). This work provides not only initial information for breeding aphid-resistant pepper varieties, but also forms the basis for future molecular analysis of gene(s) involved in aphid resistance.
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http://dx.doi.org/10.1007/s00122-019-03453-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6952328PMC
January 2020

Shoot sodium exclusion in salt stressed barley (Hordeum vulgare L.) is determined by allele specific increased expression of HKT1;5.

J Plant Physiol 2019 Oct 26;241:153029. Epub 2019 Aug 26.

Wageningen University and Research, Plant Breeding, PO Box 386, 6700 AJ, Wageningen, the Netherlands.

High affinity potassium transporters (HKT) are recognized as important genes for crop salt tolerance improvement. In this study, we investigated HvHKT1;5 as a candidate gene for a previously discovered quantitative trait locus that controls shoot Na and Na/K ratio in salt-stressed barley lines on a hydroponic system. Two major haplotype groups could be distinguished for this gene in a barley collection of 95 genotypes based on the presence of three intronic insertions; a designated haplotype group A (HGA, same as reference sequence) and haplotype group B (HGB, with insertions). HGB was associated with a much stronger root expression of HKT1;5 compared to HGA, and consequently higher K and lower Na and Cl concentrations and a lower Na/K ratio in the shoots three weeks after exposure to 200 mM NaCl. Our experimental results suggest that allelic variation in the promoter region of the HGB gene is linked to the three insertions may be responsible for the observed increase in expression of HvHKT1;5 alleles after one week of salt stress induction. This study shows that in barley - similar to wheat and rice - HKT1;5 is an important contributor to natural variation in shoot Na exclusion.
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http://dx.doi.org/10.1016/j.jplph.2019.153029DOI Listing
October 2019

Outlook for coeliac disease patients: towards bread wheat with hypoimmunogenic gluten by gene editing of α- and γ-gliadin gene families.

BMC Plant Biol 2019 Aug 1;19(1):333. Epub 2019 Aug 1.

Wageningen University and Research, Plant Breeding, Wageningen, The Netherlands.

Background: Wheat grains contain gluten proteins, which harbour immunogenic epitopes that trigger Coeliac disease in 1-2% of the human population. Wheat varieties or accessions containing only safe gluten have not been identified and conventional breeding alone struggles to achieve such a goal, as the epitopes occur in gluten proteins encoded by five multigene families, these genes are partly located in tandem arrays, and bread wheat is allohexaploid. Gluten immunogenicity can be reduced by modification or deletion of epitopes. Mutagenesis technologies, including CRISPR/Cas9, provide a route to obtain bread wheat containing gluten proteins with fewer immunogenic epitopes.

Results: In this study, we analysed the genetic diversity of over 600 α- and γ-gliadin gene sequences to design six sgRNA sequences on relatively conserved domains that we identified near coeliac disease epitopes. They were combined in four CRISPR/Cas9 constructs to target the α- or γ-gliadins, or both simultaneously, in the hexaploid bread wheat cultivar Fielder. We compared the results with those obtained with random mutagenesis in cultivar Paragon by γ-irradiation. For this, Acid-PAGE was used to identify T1 grains with altered gliadin protein profiles compared to the wild-type endosperm. We first optimised the interpretation of Acid-PAGE gels using Chinese Spring deletion lines. We then analysed the changes generated in 360 Paragon γ-irradiated lines and in 117 Fielder CRISPR/Cas9 lines. Similar gliadin profile alterations, with missing protein bands, could be observed in grains produced by both methods.

Conclusions: The results demonstrate the feasibility and efficacy of using CRISPR/Cas9 to simultaneously edit multiple genes in the large α- and γ-gliadin gene families in polyploid bread wheat. Additional methods, generating genomics and proteomics data, will be necessary to determine the exact nature of the mutations generated with both methods.
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http://dx.doi.org/10.1186/s12870-019-1889-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6670228PMC
August 2019

The AvrSen1 Triggers a Hypersensitive Response in Potatoes While Natural Variants Evade Detection.

Mol Plant Microbe Interact 2019 Nov 17;32(11):1536-1546. Epub 2019 Sep 17.

Wageningen University and Research, Plant Breeding.

is an obligate biotrophic fungus of division Chytridiomycota. It causes potato wart disease, has a worldwide quarantine status and is included on the Health and Human Services and United States Department of Agriculture Select Agent list. isolates are grouped in pathotypes based on their ability to evade host resistance in a set of differential potato varieties. Thus far, 39 pathotypes are reported. A single dominant gene () governs pathotype 1 (D1) resistance and we anticipated that the underlying molecular model would involve a pathogen effector (AvrSen1) that is recognized by the host. The -specific secretome of 14 isolates representing six different pathotypes was screened for effectors specifically present in pathotype 1 (D1) isolates but absent in others. We identified a single candidate. Expression of this candidate in potato plants showed a specific hypersensitive response (HR), which cosegregated with the resistance in potato populations. No HR was obtained with truncated genes found in pathotypes that evaded recognition by . These findings established that our candidate gene was indeed The is a single-copy gene and encodes a 376-amino-acid protein without predicted function or functional domains, and is the first effector gene identified in Chytridiomycota, an extremely diverse yet underrepresented basal lineage of fungi.
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http://dx.doi.org/10.1094/MPMI-05-19-0138-RDOI Listing
November 2019

Comparative Subsequence Sets Analysis (CoSSA) is a robust approach to identify haplotype specific SNPs; mapping and pedigree analysis of a potato wart disease resistance gene .

Plant Methods 2019 29;15:60. Epub 2019 May 29.

Wageningen UR Plant Breeding, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands.

Background: Standard strategies to identify genomic regions involved in a specific trait variation are often limited by time and resource consuming genotyping methods. Other limiting pre-requisites are the phenotyping of large segregating populations or of diversity panels and the availability and quality of a closely related reference genome. To overcome these limitations, we designed efficient Comparative Subsequence Sets Analysis (CoSSA) workflows to identify haplotype specific SNPs linked to a trait of interest from Whole Genome Sequencing data.

Results: As a model, we used the resistance to pathotypes 2, 6 and 18 that co-segregated in a tetraploid full sib population. Genomic DNA from both parents, pedigree genotypes, unrelated potato varieties lacking the wart resistance traits and pools of resistant and susceptible siblings were sequenced. Set algebra and depth filtering of subsequences (-mers) were used to delete unlinked and common SNPs and to enrich for SNPs from the haplotype(s) harboring the resistance gene(s). Using CoSSA, we identified a major and a minor effect locus. Upon comparison to the reference genome, it was inferred that the major resistance locus, referred to as , was located on the north arm of chromosome 11 between 1,259,552 and 1,519,485 bp. Furthermore, we could anchor the unanchored superscaffold DMB734 from the potato reference genome to a synthenous interval. CoSSA was also successful in identifying in a reference genome independent way thanks to the de novo assembly of paired end reads matching haplotype specific -mers. The de novo assembly provided more R haplotype specific polymorphisms than the reference genome corresponding region. CoSSA also offers possibilities for pedigree analysis. The origin of was traced back until Ora. Finally, the diagnostic power of the haplotype specific markers was shown using a panel of 56 tetraploid varieties.

Conclusions: CoSSA is an efficient, robust and versatile set of workflows for the genetic analysis of a trait of interest using WGS data. Because the WGS data are used without intermediate reads mapping, CoSSA does not require the use of a reference genome. This approach allowed the identification of and the design of haplotype specific, diagnostic markers.
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http://dx.doi.org/10.1186/s13007-019-0445-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6540404PMC
May 2019

Quantifying the Power and Precision of QTL Analysis in Autopolyploids Under Bivalent and Multivalent Genetic Models.

G3 (Bethesda) 2019 07 9;9(7):2107-2122. Epub 2019 Jul 9.

Plant Breeding, Wageningen University & Research, Droevendaalsesteeg 1, P.O. Box 386, 6700 AJ Wageningen, The Netherlands

New genotyping technologies, offering the possibility of high genetic resolution at low cost, have helped fuel a surge in interest in the genetic analysis of polyploid species. Nevertheless, autopolyploid species present extra challenges not encountered in diploids and allopolyploids, such as polysomic inheritance or double reduction. Here we investigate the power and precision of quantitative trait locus (QTL) analysis in outcrossing autopolyploids, comparing the results of a model that assumes random bivalent chromosomal pairing during meiosis to one that also allows for multivalents and double reduction. Through a series of simulation studies we found that marginal gains in QTL detection power are achieved using the double reduction model when multivalent pairing occurs. However, when exploring the effect of variable genotypic information across parental homologs, we found that both QTL detection power and precision require high and uniform genotypic information contents. This effect far outweighed considerations regarding bivalent or multivalent pairing (and double reduction) during meiosis. We propose that autopolyploid QTL studies be accompanied by both marker coverage information and per-homolog genotypic information coefficients (GIC). Application of these methods to an autotetraploid potato ( L.) mapping population confirmed our ability to locate and dissect QTL in highly heterozygous outcrossing autotetraploid populations.
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http://dx.doi.org/10.1534/g3.119.400269DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6643892PMC
July 2019

Source-Sink Regulation Is Mediated by Interaction of an FT Homolog with a SWEET Protein in Potato.

Curr Biol 2019 04 21;29(7):1178-1186.e6. Epub 2019 Mar 21.

Plant Breeding, Wageningen University & Research, P.O. Box 386, 6700 AJ Wageningen, the Netherlands. Electronic address:

Potato plants form tuberous storage organs on underground modified stems called stolons. Tubers are rich in starch, proteins, and other important nutrients, making potato one of the most important staple food crops. The timing of tuber development in wild potato is regulated by day length through a mechanism that is closely related to floral transition [1, 2]. Tuberization is also known to be regulated by the availability of assimilates, in particular sucrose, the transported form of sugar, required for starch synthesis. During the onset of tuber development, the mode of sucrose unloading switches from apoplastic to symplastic [3]. Here, we show that this switch may be mediated by the interaction between the tuberization-specific FT homolog StSP6A and the sucrose efflux transporter StSWEET11 [4]. The binding of StSP6A to StSWEET11 blocked the leakage of sucrose to the apoplast, and is therefore likely to promote symplastic sucrose transport. The direct physical interaction between StSWEET11 and StSP6A proteins represents a link between the sugar and photoperiodic pathways for the regulation of potato tuber formation. Our data suggest that a previously undiscovered function for the FT family of proteins extends their role as mobile signals to mediators of source-sink partitioning, opening the possibility for modifying source-sink interactions.
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http://dx.doi.org/10.1016/j.cub.2019.02.018DOI Listing
April 2019