Artem Pankin

Max Planck Institute for Plant Breeding Research

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Maria von Korff

Heinrich Heine University Düsseldorf

ЭЕ

Э. Е. Хавкин

All-Russian Scientific Research Institute of Food Biotechnology

МА

М. А. Кузнецова

Russian Research Institute for Phytopathology

ЕА

Е. А. Соколова

Stavropol State Agrarian University

ЕВ

Е. В. Рогозина

N.I. Vavilov Research Institute of Plant Industry

Richard W. Jones

Met Office

Seth J Davis

University of York

I. N. Kozlovskaya

Irkutsk State Medical University

S. Yu. Spiglazova

Russian Research Institute for Phytopathology

Elena A. Kinash

Cooperative Institutions

Max Planck Institute for Plant Breeding Research

Max Planck Society

Cluster of Excellence on Plant Sciences

Heinrich Heine University Düsseldorf

University of Cologne

All-Russian Scientific Research Institute of Food Biotechnology

Federal Agency for Scientific Organizations

Russian Research Institute for Phytopathology

Russian Academy of Sciences

Russian State Agrarian University - Moscow Timiryazev Agricultural Academy

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Population and Evolutionary Genetics Subfamily-specific functionalization of diversified immune receptors in wild barley

bioRxiv (Cold Spring Harbor Laboratory) (2018)

Takaki Maekawa Barbara Kracher Isabel M. L. Saur Makoto Yoshikawa-Maekawa Ronny Kellner

Abstract Gene-for-gene immunity between plants and host-adapted pathogens is often linked to population-level diversification of immune receptors encoded by disease resistance ( R ) genes. The complex barley ( Hordeum vulgare L.) R gene locus Mildew Locus A ( Mla ) provides isolate-specific resistance against the powdery mildew fungus Blumeria graminis f. sp. hordei ( Bgh ) and has been introgressed into modern barley cultivars from diverse germplasms, including the wild relative H. spontaneum . Known Mla disease resistance specificities to Bgh appear to encode allelic variants of the R Gene Homolog 1 (RGH1) family of nucleotide-binding domain and leucine-rich repeat (NLR) proteins. To gain insights into Mla diversity in wild barley populations, we here sequenced and assembled the transcriptomes of 50 accessions of H. spontaneum representing nine populations distributed throughout the Fertile Crescent. The assembled Mla transcripts exhibited rich sequence diversity, which is linked neither to geographic origin nor population structure. Mla transcripts in the tested H. spontaneum accessions could be grouped into two similar-sized subfamilies based on two major N-terminal coiled-coil signaling domains that are both capable of eliciting cell death. The presence of positively selected sites, located mainly in the C-terminal leucine-rich repeats of both MLA subfamilies, together with the fact that both coiled-coil signaling domains mediate cell death, implies that the two subfamilies are actively maintained in the host population. Unexpectedly, known MLA receptor variants that confer Bgh resistance belong exclusively to one subfamily. Thus, signaling domain divergence, potentially to distinct pathogen populations, is an evolutionary signature of functional diversification of an immune receptor.

Blumeria graminis

R gene

Subfamily

10.1101/352278

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Searching among wild Solanum species for homologues of RB/Rpi-blb1 gene conferring durable late blight resistance [Conference poster].

Artem Pankin Е. А. Соколова Е. В. Рогозина М. А. Кузнецова K. L. Deahl

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Genome‐specific SCAR markers help solve taxonomy issues: A case study with Sinapis arvensis (Brassiceae, Brassicaceae)

American Journal of Botany (2011)

Artem Pankin Э. Е. Хавкин

• Premise of the study: Traditional taxonomy and nomenclature of Brassiceae (Brassicaceae) species do not reflect their phylogeny. Revision of the species and generic limits supported by extensive molecular data seems crucial. • Methods and Results: Genome‐specific polymorphisms extracted from non‐coding and coding sequences were used to develop 14 s equence c haracterized a mplified r egion (SCAR) markers specific for the Brassica B genome. These SCARs were verified against 77 accessions of six U‐triangle Brassica species and used to screen 23 accessions of seven wild Brassiceae species to test for their cross‐species amplification. SCARs were found in all B‐genome Brassica species and also in Sinapis arvensis . • Conclusions: SCAR markers can be employed for discerning B‐genome chromosomes in Brassica species and S. arvensis to reliably identify B‐genome species and their natural hybrids. The combined molecular evidence supports the suggestion to revise the generic limits of Brassica and Sinapis .

Sinapis

Brassicaceae

10.3732/ajb.1000422

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LATE BLIGHT RESISTANCE OF SOLANUM SPECIES AND POTATO HYBRIDS: THE EVIDENCE FROM COUPLED PHYTOPATHOLOGICAL AND MOLECULAR STUDY

Е. В. Рогозина М. В. Патрикеева М. А. Кузнецова S. Yu. Spiglazova I. N. Kozlovskaya

The panel of wild Solanum species and potato hybrid clones was studied by coupled phytopathological and SCAR-marker analyses. Late blight (LB) resistance was assessed in individual plants under the field conditions and in the laboratory, with the detached-leaf test. The novel lines derived from previously unexplored sources of LB resistance among the Bolivian diploid species S. alandiae manifested a successful field resistance in the trials through two epidemic years. SCAR markers were developed using the R1, R3a and RB gene sequences. By screening wild Solanum species and clones of potato hybrids after natural and artificial infestation by P. infestans, we established that the presence of SCAR markers R1-1205 was significantly related to LB resistance. This evidence suggests the practicability of employing this marker as a breeding tool for early prediction of LB resistance in a wide range of Solanum germplasms.

Phytophthora infestans

Solanum tuberosum

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Potato resistance to late blight as related to the R1 and R3 genes introgressed from Solanum demissum [Conference poster].

Э. Е. Хавкин Е. А. Соколова М. П. Бекетова Artem Pankin М. А. Кузнецова

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SCAR markers of the R-genes and germplasm of wild Solanum species for breeding late blight-resistant potato cultivars

Plant Genetic Resources (2011)

Е. А. Соколова Artem Pankin Maria Beketova М. А. Кузнецова S. Yu. Spiglazova

New races of Phytophthora infestans rapidly defeat potato late blight (LB) resistance based on Solanum demissum germplasm, and breeders search for new sources of durable LB resistance. We developed and verified six sequence characterized amplified region markers recognizing the race-specific genes R1 and R3 of S. demissum and the broad-spectrum resistance gene RB of S. bulbocastanum and the germplasms of these species and used them to screen 209 accessions of 21 wild Solanum species. In addition to S . demissum , homologues of R1 and R3 were found in several species of series Demissa, Longipedicellata and diploid Tuberosa ; R3 homologues were also detected in S. bulbocastanum, S. cardiophyllum and S. ehrenbergii. The RB homologues were found in a wider range of Solanum species. The markers of R1 and R3 genes reliably discerned between germplasms of S. tuberosum ssp. tuberosum and wild sources of LB resistance. Following introgression, the species-specific markers of demissum and bulbocastanum germplasm were rapidly lost, whereas the markers of R1 and R3 genes lasted through several meiotic generations and were maintained at high frequencies in modern potato cultivars. The presence of these markers in demissoid potato cultivars was significantly associated with LB resistance, presuming that both genes contribute to overall defence response.

Phytophthora infestans

Germ plasm

Introgression

Solanum tuberosum

10.1017/s1479262111000347

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Co-evolution of methods and thoughts in cereal domestication studies: a tale of barley (Hordeum vulgare)

Current Opinion in Plant Biology (2016)

Artem Pankin Maria von Korff

Five major cereals such as wheat, rice, maize, barley and sorghum were among the first Neolithic crops that facilitated the establishment of the early agricultural societies. Since then they have remained the staple source of calories for the majority of the human population. Ample archaeological and molecular evidence has provided important insights into the domestication history of cereals but the debates on the origin of cereal crops are still far from resolved. Here, we review the recent advances in applying genome sequencing technologies for deciphering the history of cereal domestication. As a model example, we demonstrate that the evolution of thoughts on barley domestication closely followed the development of views on the rise of agriculture in the Near East in general and greatly accelerated with the advent of the genomic technologies and resources available for barley research.

10.1016/j.pbi.2016.12.001

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Reduced representation sequencing in barley (Hordeum vulgare L.): domestication genomics and rapid gene identification

Artem Pankin

Recent advances in barley genomics made it feasible to explore genetic diversity in a large- genome cereal and its wild relative on an unprecedented scale. Reduction of the barley genome complexity by reduced representation sequencing is a cost-efficient approach to survey genetic diversity in multiple genotypes in the context of adaptation and domestication. Moreover, reduced representation sequencing generates genome-wide panels of polymorphisms, thus enabling the application of mapping-by-sequencing approaches in cereals, which has been gaining ground as a rapid method to fine-map candidate genes underlying agronomic traits. In the first part of this study, I focused on understanding the genetic architecture of the barley domestication syndrome and underlying processes modulating diversity in wild and domesticated forms. To this end, I interrogated ~330,000 SNPs in a set of 433 diverse wild and cultivated barley genotypes using a custom designed reduced representation sequencing assay. The SNPs originated from ~ 12,800 loci, enriched for homologs of flowering time, of meristem and inflorescence development, and of domestication-related genes. The diversity analysis identified an unexpectedly high rate of admixture in both wild and domesticated forms, with the latter case predominantly restricted to the landrace genotypes. I found evidence of a severe domestication bottleneck resulting in loss of genetic diversity and maintenance of extended haplotype blocks in strong linkage disequilibrium. Selection scans identified multiple targets of selection related to the crucial domestication syndrome traits. For examples, several tests identified a sweep that occurred around the genes involved in the non-brittle rachis phenotype. The signatures of selection were found in the homologs of genes implicated in the regulation of photoperiodic flowering, gibberellin synthesis and seed dormancy. This map of barley genetic variation will inform future evolutionary and genome-wide association studies and support the advancement of barley breeding. In the second chapter, I employed another reduced representation sequencing approach, the whole-exome sequencing, in combination with the mapping-by-sequencing algorithm. Using this toolbox, I identified the red/far-red light photoreceptor HvPHYTOCHROME C (HvPHYC), carrying a mutation in a conserved region of the GAF domain, as a candidate underlying the early maturity 5 (eam5) locus in barley. I fine-mapped the gene using the SHOREmap algorithm applied on the whole-exome capture data from bulked early flowering segregants derived from a backcross of the Bowman(eam5) 5introgression line. Phytochromes play an important role in light signaling and photoperiodic control of flowering time in plants. Here, I show that the eam5 interacts with the photoperiod response gene PHOTOPERIOD-H1 (Ppd-H1) to accelerate flowering under non-inductive short days. The results accompanying my study suggest that HvPHYC participates in the transmission of light signals to the circadian clock and thus modulates light-dependent processes such as photoperiodic regulation of flowering. The diversity analysis indicates enrichment of the HvPHYC-eam5 allele in barley cultivars from Japan despite the strong effect of this mutation on the barley clock. This invites further research into comparing physiological effects and the overall significance of the circadian clock on plant adaptation.

Nucleotide diversity

Population genomics

Linkage Disequilibrium

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Global Transcriptome Profiling of Developing Leaf and Shoot Apices Reveals Distinct Genetic and Environmental Control of Floral Transition and Inflorescence Development in Barley

The Plant Cell (2015)

Benedikt Digel Artem Pankin Maria von Korff

Timing of the floral transition and inflorescence development strongly affect yield in barley (Hordeum vulgare). Therefore, we examined the effects of daylength and the photoperiod response gene PHOTOPERIOD1 (Ppd-H1) on barley development and analyzed gene expression changes in the developing leaves and main shoot apices (MSAs) of barley by RNA sequencing. The daylength sensitivity of MSA development had two phases, floret primordia initiated under long and short days, whereas successful inflorescence development occurred only under long days. The transcripts associated with floral transition were largely regulated independently of photoperiod and allelic variation at Ppd-H1. The photoperiod- and Ppd-H1-dependent differences in inflorescence development and flower fertility were associated with the induction of barley FLOWERING LOCUS T orthologs: FT1 in leaves and FT2 in MSAs. FT1 expression was coregulated with transcripts involved in nutrient transport, carbohydrate metabolism, and cell cycle regulation, suggesting that FT1 might alter source-sink relationships. Successful inflorescence development correlated with upregulation of FT2 and transcripts related to floral organ development, phytohormones, and cell cycle regulation. Identification of photoperiod and stage-specific transcripts gives insights into the regulation of reproductive development in barley and provides a resource for investigation of the complexities of development and yield in temperate grasses.

Primordium

10.1105/tpc.15.00203

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Are simple Phytophthora infestans races really that simple

Artem Pankin Elena A. Kinash I. N. Kozlovskaya М. А. Кузнецова Э. Е. Хавкин

SUMMARY Allelic diversity of the IpiO gene encoding the effector recognised by Rpi‐blb1/RB gene from S. bulbocastanum and S. stoloniferum was assessed by PCR screening and sequencing in 15 races (1, 3, 4, 10, 11, 1.2, 1.3, 1.4, 2.4, 3.4, 1.11, 1.2.3, 1.2.4, 1.3.4, and 1.2.3.4) maintained in the collection of the Institute of Phytopathology. IpiO locus was present in all these isolates. Phylogenetic analysis demonstrated that IpiO alleles from races 3 and 4 belonged to the classes I and II recognised by R pi-blb 1/RB. It follows that these “simple” races exhibit simple virulence patterns on potato comprising only R1-R11 genes from S. demissum . Growing interest in exploiting exotic Solanum germplasm in potato breeding is an incentive to reconsider and unambiguously redefine the terms “simple” and “complex” race. KEYWORDS Phytophthora infestans , Solanum , potato, late blight resistance, effectors, simple races INTRODUCTION Approaches to describe the diversity of P. infestans Various methods and protocols were developed to identify, distinguish, and classify

Phytophthora infestans

Germ plasm

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