Genetic Resources of Cereal and Oilseed Crops for Sustainable Breeding and Food Security

A special issue of Plants (ISSN 2223-7747). This special issue belongs to the section "Plant Genetics, Genomics and Biotechnology".

Deadline for manuscript submissions: closed (20 May 2022) | Viewed by 34043

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N. I. Vavilov All-Russian Institute of Plant Genetic Resources, 42-44 Bolshaya Morskaya Street, St. Petersburg 190000, Russia
Interests: genetic diversity; seed storage proteins (polymorphism, genetic control, genomic organization); cytoplasmic male sterility–restoration of fertility (CMS-Rf) genetic systems; theoretical and applied aspects of interspecific hybridization (with special emphasis on sunflower)
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Guest Editor
1. Laboratory of Cell and Genomic Technologies, Russian Potato Research Center, 23 Lorkh Str., Kraskovo, 140051 Moscow Region, Russia
2. Laboratory of Plant Genetics, N.I.Vavilov Institute of General Genetics, Russian Academy of Sciences. 119334 Moscow, Russia
Interests: crop genetics and genomics; plant breeding; biodiversity and evolution
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Department of Genetics, Federal Research Center, The N. I. Vavilov All-Russian Institute of Plant Genetic Resources, 42,44 Bolshaya Morskaya Street, 19000 St.Petersburg, Russia
Interests: cultivated plants and wild relatives; genetic diversity; plant breeding; resistance to harmful organisms
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Special Issue Information

Dear Colleagues,

Cereal and oilseed crops are indispensable for existence of humankind. They are ubiquitously used for human and animal nutrition, medicinal purposes, obtaining ecologically friendly materials. Genebanks play an important role in conservation and the study of plant genetic resources. Collections of genetic resources of cereal and oilseed crops conserved in Genebanks include thousands of accessions representing old and modern varieties, landraces, breeding lines, and also wild species that can be used for breeding new genotypes possessing valuable traits.

Due to the domestication “bottleneck” effect in human history, the genetic basis of a number of cereal and oilseed crop species is comparatively narrow. Hybridization with landraces and wild species significantly facilitates broadening genetic diversity of breeding material for resistance to harmful organisms and tolerance to abiotic stressors. Distant hybridization may bring completely new traits that can revolutionize crop breeding and production. As an example, the phenomenon of cytoplasmic male sterility (CMS) and fertility restoration, which is an important factor of speciation during plant evolution, has gained new significance as the basis for seed production in heterotic hybrid breeding.

Dr. Irina N. Anisimova
Dr. Svetlana Goryunova
Dr. Eugene Radchenko
Guest Editors

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Keywords

  • Keywords: cereal and oilseed plants
  • genetics and genomics
  • biodiversity and evolution
  • distant hybridization
  • agronomically important traits
  • CMS-Rf genetic systems

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Related Special Issue

Published Papers (11 papers)

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Research

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17 pages, 2191 KiB  
Article
Phylogenetic Analysis and Flower Color Evolution of the Subfamily Linoideae (Linaceae)
by Alejandra Villalvazo-Hernández, Mireya Burgos-Hernández and Dolores González
Plants 2022, 11(12), 1579; https://doi.org/10.3390/plants11121579 - 15 Jun 2022
Cited by 2 | Viewed by 2595
Abstract
The taxonomy of the subfamily Linoideae at the intergeneric and section levels has been questioned throughout the years, and the evolution of floral characters remains poorly understood. In particular, the evolution of flower color is still uncertain, despite its ecological importance and being [...] Read more.
The taxonomy of the subfamily Linoideae at the intergeneric and section levels has been questioned throughout the years, and the evolution of floral characters remains poorly understood. In particular, the evolution of flower color is still uncertain, despite its ecological importance and being one of the most variable and striking traits in Angiospermae. We evaluated the phylogenetic relationships of the genera and sections and used the phylogeny to reconstruct the ancestral state of flower color. The results suggest reevaluating the taxonomic status of segregated genera and re-incorporating them into Linum. Four of the five sections currently accepted were recovered as monophyletic (Cathartolinum, Dasylinum, Linum, and Syllinum). We propose accepting the section Stellerolinon and reevaluating Linopsis, whose representatives were recovered in three separate clades. The ancestral flower color for Linoideae was yellow-white. The flower colors purple and yellow-white were recovered at the deepest nodes of the two main clades. Pink, blue, and red colors were the most recent to evolve. These results appear to be related to diversification events, biogeographical history, and ecological aspects of the subfamily. Our reconstruction constitutes the first plausible scenario that explores the evolution of flower color, leading to new testable hypotheses for future research on the flax group. Full article
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12 pages, 2974 KiB  
Article
A Genome-Wide Association Study Identifying Single-Nucleotide Polymorphisms for Iron and Zinc Biofortification in a Worldwide Barley Collection
by Solange Nyiraguhirwa, Zahra Grana, Hassan Ouabbou, Driss Iraqi, Mohammed Ibriz, Sujan Mamidi and Sripada M. Udupa
Plants 2022, 11(10), 1349; https://doi.org/10.3390/plants11101349 - 19 May 2022
Cited by 11 | Viewed by 2405
Abstract
Micronutrient deficiency affects half of the world’s population, mostly in developing countries. Severe health issues such as anemia and inadequate growth in children below five years of age and pregnant women have been linked to mineral deficiencies (mostly zinc and iron). Improving the [...] Read more.
Micronutrient deficiency affects half of the world’s population, mostly in developing countries. Severe health issues such as anemia and inadequate growth in children below five years of age and pregnant women have been linked to mineral deficiencies (mostly zinc and iron). Improving the mineral content in staple crops, also known as mineral biofortification, remains the best approach to address mineral malnutrition. Barley is a staple crop in some parts of the world and is a healthy choice since it contains β-glucan, a high dietary protein. Barley mineral biofortification, especially with zinc and iron, can be beneficial since barley easily adapts to marginalized areas and requires less input than other frequently consumed cereals. In this study, we analyzed zinc and iron content in 496 barley samples. The samples were genotyped with an Illumina 50 K SNP chip. Genome-wide association studies (GWAS) identified 62 SNPs and 68 SNPs (p < 0.001) associated with iron and zinc content in grains, respectively. After a Bonferroni correction (p < 0.005), there were 12 SNPs (single-nucleotide polymorphism) associated with Zn and 6 for iron. SNP annotations revealed proteins involved in membrane transport, Zn and Fe binding, linked to nutrient remobilization in grains. These results can be used to develop biofortified barley via marker-assisted selection (MAS), which could alleviate mineral malnutrition. Full article
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11 pages, 2089 KiB  
Article
Effectiveness of Leaf Rust Resistance Genes in the Adult and Juvenile Stages in Southern Russia in 2011–2020
by Galina Volkova, Olga Kudinova, Olga Vaganova and Valeria Agapova
Plants 2022, 11(6), 793; https://doi.org/10.3390/plants11060793 - 16 Mar 2022
Cited by 5 | Viewed by 2388
Abstract
Puccinia triticina Erikss. is a causative agent of wheat leaf rust spread worldwide. Wheat rust is a major disease on wheat in southern regions of Russia, which are leaders in grain production and have favorable conditions for pathogen development. In this paper we [...] Read more.
Puccinia triticina Erikss. is a causative agent of wheat leaf rust spread worldwide. Wheat rust is a major disease on wheat in southern regions of Russia, which are leaders in grain production and have favorable conditions for pathogen development. In this paper we studied the effectiveness of 52 NILs of cv. Thatcher with Lr genes in field trials and 41 NILs—in the juvenile phase in a greenhouse during 2011–2020. We conclude that the lines with Lr9, Lr42 and Lr43+24 genes remained immune in the adult phase during ten years of research. Lines with Lr genes: 19, 24, 29, 36, 37, 38, 43, 45, 47, 50 showed efficiency in field tests (1–5 R on the CIMMYT scale). No immune lines to Puccinia triticina were registered in the juvenile phase during 2011–2020. The line with the Lr9 gene remained immune up to 2020; Lr19 and Lr41—up to 2015; Lr42—up to 2018, and Lr50—up to 2019. In 2020, there was an increase of P. triticina isolates with virulence to Thatcher lines with Lr: 9, 14a, 16, 19, 21, 28, 30, 33, 40, 45, W, 50. Additionally, we registered a change in infection types towards more susceptible in isogenic Lr gene lines: 1, 2a, 12, 14b, 15, 18, 20, 23, 25, 28, 29, 32, 35, 36, 37, 38, 40, 44, 45 in the field. A sharp increase in the frequencies of virulent isolates was recorded in 2018–2020 due to unfavorable weather in the growing seasons. This indicates the ability of a dangerous pathogen to rapidly evolve in response to biotic and abiotic stresses. Therefore, annual monitoring of the reaction of isogenic lines, selected released varieties and the study of the virulence of the phytopathogen are important measures necessary to prevent and control leaf rust in grain-producing regions of the world. Full article
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25 pages, 4763 KiB  
Article
Features of Profiles of Biologically Active Compounds of Primary and Secondary Metabolism of Lines from VIR Flax Genetic Collection, Contrasting in Size and Color of Seeds
by Elizaveta A. Porokhovinova, Tatyana V. Shelenga, Yulia A. Kerv, Valentina I. Khoreva, Alexey V. Konarev, Tamara V. Yakusheva, Andrey V. Pavlov, Anastasia A. Slobodkina and Nina B. Brutch
Plants 2022, 11(6), 750; https://doi.org/10.3390/plants11060750 - 11 Mar 2022
Cited by 6 | Viewed by 2933
Abstract
Flax is one of the oldest oil crops, but only since the end of the twentieth century nutritional use of its whole seeds and flour has been resumed. This crop has been evaluated for its oil fatty acid composition, content of sterols and [...] Read more.
Flax is one of the oldest oil crops, but only since the end of the twentieth century nutritional use of its whole seeds and flour has been resumed. This crop has been evaluated for its oil fatty acid composition, content of sterols and tocopherols, carbohydrate composition of mucilage, but a comprehensive study has never been carried out, so the aim of the work was to identify differences in the metabolomic profiles of flax lines contrasting in color and size of seeds. The biochemical composition of seeds from 16 lines of the sixth generation of inbreeding was tested using gas chromatography coupled with mass spectrometry. In total, more than 90 compounds related to sugars (78% of the identified substances), free fatty acids (13%), polyatomic alcohols (5%), heterocyclic compounds, free amino acids, phytosterols and organic acids (no more than 2.5% in total) were identified. Statistical analyses revealed six main factors. The first is a factor of sugar content; the second one affects most of organic acids, as well as some free fatty acids, not related to reserve ones, the third factor is related to compounds that play a certain role in the formation of “storage” substances and resistance to stress, the fourth factor is influencing free polar amino acids, some organic and free fatty acids, the fifth one is a factor of phenolic compounds, the sixth factor combined substances not included in the first five groups. Factor analysis made it possible to differentiate all 16 lines, 10 of which occupied a separate position by one or two factors. Interestingly, the first two factors with the highest loads (20 and 15% of the total variability, respectively) showed a separate position of the gc-432 line, which differed from the others, not only by chemical composition, but also by the phenotype of the seeds, while gc-159 differed from the rest ones by the complex of organic acids and other substances taking about 1% of the extracted substances of the seed. Thus, the analysis of metabolomic profiles is promising for a comprehensive assessment of the VIR flax genetic collection, which has wide biochemical diversity. Full article
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17 pages, 1594 KiB  
Article
Heritability and Associations among Grain Yield and Quality Traits in Quality Protein Maize (QPM) and Non-QPM Hybrids
by Isaac Kodzo Amegbor, Angeline van Biljon, Nemera Shargie, Amsal Tarekegne and Maryke T. Labuschagne
Plants 2022, 11(6), 713; https://doi.org/10.3390/plants11060713 - 8 Mar 2022
Cited by 18 | Viewed by 2633
Abstract
Maize (Zea mays L.) is the main staple cereal food crop cultivated in southern Africa. Interactions between grain yield and biochemical traits can be useful to plant breeders in making informed decisions on the traits to be considered in breeding programs for [...] Read more.
Maize (Zea mays L.) is the main staple cereal food crop cultivated in southern Africa. Interactions between grain yield and biochemical traits can be useful to plant breeders in making informed decisions on the traits to be considered in breeding programs for high grain yield and enhanced quality. The objectives of this study were to estimate the heritability of grain yield and its related traits, as well as quality traits, and determine the association between quality protein maize (QPM) with non-QPM crosses. Grain yield, and agronomic and quality trait data were obtained from 13 field trials in two countries, for two consecutive seasons. Significant genotypic and phenotypic correlations were recorded for grain yield with protein content (rG = 0.38; rP = 0.25), and tryptophan with oil content (rG = 0.58; rP = 0.25), and negative rG and rP correlations were found for protein with tryptophan content and grain yield with tryptophan content. Path analysis identified ear aspect, ears per plant, and starch as the major traits contributing to grain yield. It is recommended that ear aspect should be considered a key secondary trait in breeding for QPM hybrids. The negative association between grain yield and tryptophan, and between protein and tryptophan, will make it difficult to develop hybrids with high grain yield and high tryptophan content. Hence, it is recommended that gene pyramiding should be considered for these traits. Full article
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12 pages, 965 KiB  
Article
Adaptability and Stability of Safflower Genotypes for Oil Production
by Sebastião Soares de Oliveira Neto, Douglas Mariani Zeffa, Gustavo Henrique Freiria, Tiago Zoz, Carlos Jorge da Silva, Maurício Dutra Zanotto, Renato Lustosa Sobrinho, Saud A. Alamri, Mohammad K. Okla and Hamada AbdElgawad
Plants 2022, 11(5), 708; https://doi.org/10.3390/plants11050708 - 7 Mar 2022
Cited by 12 | Viewed by 3100
Abstract
The study aimed to analyze the agronomic performance of 11 safflower genotypes using adaptability and stability methods, while identifying safflower genotypes with stable behavior and a high grain yield in different environments of the Brazilian Cerrado. Ten lines and a cultivar of safflower [...] Read more.
The study aimed to analyze the agronomic performance of 11 safflower genotypes using adaptability and stability methods, while identifying safflower genotypes with stable behavior and a high grain yield in different environments of the Brazilian Cerrado. Ten lines and a cultivar of safflower were evaluated in four environments in the Brazilian conditions. Our results revealed the genotypes P30, P35, P9, P11, and P31 to be superior for grain yield and P43, P7, P11, and P31 to be superior for oil content. The lowest Wricke index, an indication of genotype stability, was observed for P9 (0.41%), which is considered the most stable genotype, followed by P35 (1.29%) and P31 (1.98%). For the predictability of the behavior of genotypes in the environments, P7 (80.85%), P35 (86.10%), P31 (85.90%), and P9 (97.42%) were considered predictable genotypes. The genotypes P11 (1045.6 kg ha−1 and 19.7%) and P21 (952.7 kg ha−1 and 20.6%) are recommended for cultivation in this region, considering both their grain yield and oil content. Safflower is viable to use out of season in the Brazilian Cerrado. The crop can generate profits for farmers and be used for oil production in periods of uncertain corn production. Full article
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23 pages, 1124 KiB  
Article
Genetic Analysis for Resistance to Sclerotinia Stem Rot, Yield and Its Component Traits in Indian Mustard [Brassica juncea (L.) Czern & Coss.]
by Manjeet Singh, Ram Avtar, Neeraj Kumar, Rakesh Punia, Ajay Pal, Nita Lakra, Nisha Kumari, Dalip Kumar, Anu Naruka, Mahavir Bishnoi, Rajbir Singh Khedwal, Raju Ram Choudhary, Anoop Singh, Ravindra Kumar Meena, Ankit Dhillon and Vivek K. Singh
Plants 2022, 11(5), 671; https://doi.org/10.3390/plants11050671 - 28 Feb 2022
Cited by 13 | Viewed by 4218
Abstract
Understanding the mode of gene action that controls seed yield and Sclerotinia stem rot resistance in Indian mustard is critical for boosting yield potential. In a line × tester mating design, ten susceptible lines and four resistant testers were used to conduct genetic [...] Read more.
Understanding the mode of gene action that controls seed yield and Sclerotinia stem rot resistance in Indian mustard is critical for boosting yield potential. In a line × tester mating design, ten susceptible lines and four resistant testers were used to conduct genetic analysis. The significance of general combining ability (GCA) and specific combining ability (SCA) variances revealed that both additive and non-additive gene actions were involved in the inheritance of Sclerotinia stem rot resistance and yield attributing traits. In addition to 1000-seed weight and number of primary and secondary branches/plant, the genotypes RH 1569 (line) and DRMR 2035 (tester) appeared to be the strongest general combiners for Sclerotinia stem rot resistance. RH 1657 × EC 597317 was the only cross among several that demonstrated a significant desired SCA value for Sclerotinia rot resistance. Regarding SCA effects for yield and component traits, the cross RH 1658 × EC 597328 performed best, with a non-significant but acceptable negative SCA effect for resistance. DRMR 2035, RH 1222-28, RH 1569, RH 1599-41, RH 1657, RH 1658, and EC 597328 are promising genotypes to use as parents in future heterosis breeding and for obtaining populations with high yield potential and greater resistance to Sclerotinia stem rot disease in Indian mustard, based on GCA effects of parents, per se performance, and SCA effects of hybrids. Days to 50% flowering, number of primary branches/plant, main shoot length, and 1000-seed weight all had a high genotypic coefficient of variability (GCV), broad-sense heritability (h2bs), and genetic advance as percent of the mean (GAM) values, as well as significant and desirable correlations and direct effects on seed yield. As a result, these traits have been recognized as the most critical selection criterion for Indian mustard breeding programs. Full article
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10 pages, 1936 KiB  
Article
Clarification of the Position of Linum stelleroides Planch. within the Phylogeny of the Genus Linum L.
by Nadezhda L. Bolsheva, Nataliya V. Melnikova, Ekaterina M. Dvorianinova, Liudmila N. Mironova, Olga Y. Yurkevich, Alexandra V. Amosova, George S. Krasnov, Alexey A. Dmitriev and Olga V. Muravenko
Plants 2022, 11(5), 652; https://doi.org/10.3390/plants11050652 - 27 Feb 2022
Cited by 5 | Viewed by 2545
Abstract
The phylogeny of members of the family Linaceae DC. ex Perleb has not been adequately studied. In particular, data on the phylogenetic relationship between Linum stelleroides Planch. and other representatives of the blue-flowered flax are very controversial. In the present work, to clarify [...] Read more.
The phylogeny of members of the family Linaceae DC. ex Perleb has not been adequately studied. In particular, data on the phylogenetic relationship between Linum stelleroides Planch. and other representatives of the blue-flowered flax are very controversial. In the present work, to clarify this issue, we obtained DNA sequences of three nuclear loci (IGS and ITS1 + 5.8S rDNA + ITS2 of the 35S rRNA gene and the 5S rRNA gene) and eight chloroplast loci (rbcL, the trnLtrnF intergenic spacer, matK, the 3′ trnK intron, ndhF, trnG, the psbAtrnH intergenic spacer, and rpl16) of 10 Linum L. species (L. stelleroides, L. hirsutum, L. perenne, L. leonii, L. lewisii, L. narbonense, L. decumbens, L. grandiflorum, L. bienne (syn. L. angustifolium), and L. usitatissimum) using high-throughput sequencing data. The phylogenetic analysis showed that L. stelleroides forms a basal branch in the blue-flowered flax clade. Previously found inconsistencies in the position of L. stelleroides and some other species in the Linaceae phylogenetic tree resulted from the erroneous species identification of some of the studied plant samples. Full article
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20 pages, 2363 KiB  
Article
Genes Associated with the Flax Plant Type (Oil or Fiber) Identified Based on Genome and Transcriptome Sequencing Data
by Liubov V. Povkhova, Nataliya V. Melnikova, Tatiana A. Rozhmina, Roman O. Novakovskiy, Elena N. Pushkova, Ekaterina M. Dvorianinova, Alexander A. Zhuchenko, Anastasia M. Kamionskaya, George S. Krasnov and Alexey A. Dmitriev
Plants 2021, 10(12), 2616; https://doi.org/10.3390/plants10122616 - 28 Nov 2021
Cited by 9 | Viewed by 2956
Abstract
As a result of the breeding process, there are two main types of flax (Linum usitatissimum L.) plants. Linseed is used for obtaining seeds, while fiber flax is used for fiber production. We aimed to identify the genes associated with the flax [...] Read more.
As a result of the breeding process, there are two main types of flax (Linum usitatissimum L.) plants. Linseed is used for obtaining seeds, while fiber flax is used for fiber production. We aimed to identify the genes associated with the flax plant type, which could be important for the formation of agronomically valuable traits. A search for polymorphisms was performed in genes involved in the biosynthesis of cell wall components, lignans, fatty acids, and ion transport based on genome sequencing data for 191 flax varieties. For 143 of the 424 studied genes (4CL, C3′H, C4H, CAD, CCR, CCoAOMT, COMT, F5H, HCT, PAL, CTL, BGAL, ABC, HMA, DIR, PLR, UGT, TUB, CESA, RGL, FAD, SAD, and ACT families), one or more polymorphisms had a strong correlation with the flax type. Based on the transcriptome sequencing data, we evaluated the expression levels for each flax type-associated gene in a wide range of tissues and suggested genes that are important for the formation of linseed or fiber flax traits. Such genes were probably subjected to the selection press and can determine not only the traits of seeds and stems but also the characteristics of the root system or resistance to stresses at a particular stage of development, which indirectly affects the ability of flax plants to produce seeds or fiber. Full article
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Review

Jump to: Research

16 pages, 301 KiB  
Review
Effectiveness of and Perspectives for the Sedimentation Analysis Method in Grain Quality Evaluation in Various Cereal Crops for Breeding Purposes
by Ilya Kibkalo
Plants 2022, 11(13), 1640; https://doi.org/10.3390/plants11131640 - 21 Jun 2022
Cited by 8 | Viewed by 2211
Abstract
The existing standardized methods for assessing the quality of marketable grain do not always meet the requirements of the breeding, such as the method’s rapidity, sufficiency of the minimum amount of experimental material, the minimal modifying influence of the external environment on the [...] Read more.
The existing standardized methods for assessing the quality of marketable grain do not always meet the requirements of the breeding, such as the method’s rapidity, sufficiency of the minimum amount of experimental material, the minimal modifying influence of the external environment on the degree of expression of a criterion, and genetic determination and heritability of the latter. One of the methods that meets these requirements is the sediment volume test. The present study offers an analysis and examples of methodological developments in relation to the assessment of winter bread wheat grain in arid regions of cultivation, as well as of winter triticale. The fluorescent probing method was used as an example for demonstrating the prospects for assessing the swelling of ground grain products of both bread and durum wheat, and for such crops with a less-strong complex of storage polymers as triticale, rye, and millet. A two-stage sedimentation procedure that allows a successful differentiation of samples has been developed for sorghum and maize grain. It is presented here alongside with methodological works on wheat from different countries of the world. Examples of the proven high reproducibility of the sediment volume test in the offspring, and its genetic determination are provided. In general, the data obtained and the material accumulated by various researchers indicate that a modification of the sedimentation method, correctly chosen for specific goals and objectives, solves the problem of assessing grain quality in breeding samples starting from early progenies. All these circumstances make the sedimentation testing the leading or most promising method for assessing grain quality when breeding of a broad range of grain crops is carried out. Full article
28 pages, 469 KiB  
Review
Genetic Resources of Cereal Crops for Aphid Resistance
by Evgeny E. Radchenko, Renat A. Abdullaev and Irina N. Anisimova
Plants 2022, 11(11), 1490; https://doi.org/10.3390/plants11111490 - 31 May 2022
Cited by 10 | Viewed by 3523
Abstract
The genetic resources of cereal crops in terms of resistance to aphids are reviewed. Phytosanitary destabilization led to a significant increase in the harmfulness of this group of insects. The breeding of resistant plant genotypes is a radical, the cheapest, and environmentally safe [...] Read more.
The genetic resources of cereal crops in terms of resistance to aphids are reviewed. Phytosanitary destabilization led to a significant increase in the harmfulness of this group of insects. The breeding of resistant plant genotypes is a radical, the cheapest, and environmentally safe way of pest control. The genetic homogeneity of crops hastens the adaptive microevolution of harmful organisms. Both major and minor aphid resistance genes of cereal plants interact with insects differentially. Therefore, rational breeding envisages the expansion of the genetic diversity of cultivated varieties. The possibilities of replenishing the stock of effective resistance genes by studying the collection of cultivated cereals, introgression, and creating mutant forms are considered. The interaction of insects with plants is subject to the gene-for-gene relationship. Plant resistance genes are characterized by close linkage and multiple allelism. The realizing plant genotype depends on the phytophage biotype. Information about the mechanisms of constitutional and induced plant resistance is discussed. Resistance genes differ in terms of stability of expression. The duration of the period when varieties remain resistant is not related either to its phenotypic manifestation or to the number of resistance genes. One explanation for the phenomenon of durable resistance is the association of the virulence mutation with pest viability. Full article
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