Сельскохозяйственная биология, 2012, № 5, с. 54-63.

doi: 10.15389/agrobiology.2012.5.54eng

УДК 633.1:631.524.86:632.7:631.522/.524

N.I. VAVILOV’s THEORY ON NATURAL IMMUNITY OF PLANTS TO HARMFUL ORGANISMS AND BREEDING OF CEREAL CROPS FOR APHID RESISTANCE

E.E. Radchenko

The data on mechanisms of cereal crops active and passive resistance to cereal aphids are presented. The specificity of interaction between the insects and host plants is discussed. The prospects for broadening of cereal genetic diversity for aphid resistance are considered. It is shown that adaptation process of harmful organisms can be slow down by means of rational territorial distribution of donors with different resistance genes in population areas of insect. The results of studies on cereal crops genetic resources for aphid resistance completely confirm the laws on natural immunity of plants to harmful organisms which were stated by N.I. Vavilov.

Keywords: cereal crops, aphids, natural immunity.

The development of intensive agriculture has significantly increased the harmfulness of aphid pests against cereal crops. Thus, in sorghum, crop losses caused by Schizaphis graminum may exceed 85% in our country (1). The potential harmfulness of aphids to cereals was evidenced by facts of recent decades: e.g., in South Africa and the USA Diuraphis noxia (Brachycolus noxius) has become the major pest of cereals crops.
Genetic homogeneity of cultivated varieties accelerates adaptive co-evolution of pests. The use of broad-spectrum pesticides often disturbs the biological balance: they cause death of entomophagous species while the mass expansion of pests. Besides, aphids can acquire the resistance to insecticides (2), and some herbicides even stimulate propagation of plant-sucking pests (3). In this view, selection of resistant plant genotypes is a radical way to combat aphids and yet most inexpensive and environmentally friendly one. Breeding cereal crops for immunity has one major purpose – to restore their genetic diversity in terms of pest resistance.
According to N.I. Vavilov (4), natural (inherited) immunity of plants to pests can be considered in terms of generic, specific and varietal immunity, because major parasites affect specific genera and species of hosts due to the divergence of hosts and parasites during an evolution. “Normal varietal immunity”, in turn, includes active (physiological) immunity associated with cellular responses of a host – various physiological and chemical reactions, and neoplastic formations, and passive immunity not related to host’s response to pest invasion. Then, the passive immunity can be structural (mechanical) – resulting from morphological and anatomical features of plant varieties, and chemical – associated with the presence of certain substances in plant tissues. The precocity developed by a host in order to avoid damaging by pests is a special category essentially unrelated to the immunity.
So, immunity is created through the interaction of many elements. Mechanisms of active and passive immunity of cereal crops to aphids are being discussed in available literature.
N.A. Mikhailova (5) assumes that Triticum monococcum is less affected by Sitobion (Macrosiphum) avenae owing to a tiled arrangement of spikelets in the ear. Fecundity of S. avenae inhabiting ear awns was found to be 22% lower than that of the pest consuming other parts of the ear (6). The largest colonies of aphids were observed by A.M. Sumarokov (7) in male inflorescences of maize, which had been closed by upper leaves for a long time but not tightly wrapped in.
In experiments of H.J.B. Lowe (8) waxless wheat lines exhibited higher resistance to S. avenae than the wax-filmed lines. It was also shown that waxless barley was much less affected by Metopolophium dirhodum (9), and waxless sorghum was less attractive for Schizaphis graminum (10).
The facts about the relationship between a pubescence and plant resistance to cereal aphids are somewhat contradictory. Many scientists suppose that thickness and length of the trichomes in wheat are not correlated with traits affecting its resistance to S. graminum (11) and Rhopalosiphum padi (12). In the authors’ experiments, long trichomes did not prevent successful feeding of R. padi. However, dense pubescence possibly limits aphid invasion: the most resistant samples Delphi 400 and Karagandinskaya 2 have dense pubescence on leaves (13). The sample PI 137739 resistant to D. noxia has long pubescence as well (14). Synthetic hexaploid barley (T. dicoccum х Aegilops tauschii) is unattractive for D. noxia  probably due to pubescence on its leaves (15).
Chemical substances produced by plants in order to protect themselves against plant-eating pests have been studied in detail. The role of secondary metabolites - terpenoids, phenols, flavonoids, alkaloids, glucosinolates etc. is being discussed.  Protein compounds, primarily inhibitors of pest hydrolases (proteinases, b-amylases, etc.) and lectins, are essentially important. These substances are present mainly in the storage organs of plants and insect damage induces their accumulation.
The resistance of winter wheat to S. avenae is closely correlated with the “toxicity index” - the ratio of the content of free phenols in the plant to free amino acids (16). Diterpene acids deterrent nutrition of S. avenae as well. Testing 11 acids has revealed a wide variation of their deterrent activity (17).
Various species of the family Gramineae with relatively high content of hydroxamic acids - 2,4-dihydroxy-7-methoxy-(2H) -1,4-benzoxazin-3(4H)-one (DIMBOA) and 2,4-dihydroxy-(2H)-1,4-benzoxazin-3(4H)-one (DIBOA) are resistant to various aphid species. The maximum content of hydroxamic acid was found in young plants of cereals (18-20). Genes responsible for the synthesis of DIMBOA and DIBOA have been identified in wheat: TaBx1-TaBx5 genes orthologous to Bx1-Bx5 genes previously detected in maize. These genes belong to wheat genomes A, B and D (respectively TaBx1A-TaBx5A, TaBx1B-TaBx5B and TaBx1D-TaBx5D). The homologs of B genome provide the largest share of hydroxamic acids in hexaploid wheat (21-23). In accordance to the Vavilov’s law of homologous series (24), it has been found that wild barley Hordeum lechleri has the genes HlBx1-HlBx5 orthologous to Bx1-Bx5 and providing synthesis of DIBOA (25).
Recently much attention is paid to the study of induced resistance of wheat to aphids (Vavilov’s term: active resistance). Using nearly isogenic lines of wheat (susceptible and resistant one with the gene Gb3 for resistance to S. graminum), Y. Weng et al. (26) have revealed a systemic resistance of plants induced by pest nutrition: invasion of D. noxia caused accumulation in plants of phenols and PR-proteins (pathogenesis-related proteins) (27, 28). It was shown that the pest induces in wheat varieties-carriers of Dn1 gene the accumulation of chitinases and β-1,3-glucanases, which are important for a hypersensitive response in plant tissue (29-31). At the same time, glycoproteins are probably the major elicitors (inducers) of plant resistance (32).
When feeding aphids are recognized by a plant, this promotes the activation of signaling systems and multiple increase in concentrations of jasmonic acid, salicylic acid, ethylene, etc. (33). For example, the aphid D. noxia is recognized through NADPH-oxidase signaling system; the pest feeding on the resistant variety Tugela DN provided a rapid accumulation of hydrogen peroxide and salicylic acid, as well as elevation of peroxidase activity in plant tissues (34, 35). In host plants colonized by D. noxia and showing the expression of Dnx gene there have been identified more than 180 genes involved in signaling and protective functions. Lipoxygenase signaling system is also important for pest recognition by a host plant (36). In the case when resistant plants-carriers of Dn7 gene were colonized by two biotypes of D. noxia, this provided activation of several signaling systems - Ca²⁺-phosphoinositol, lipoxygenase, NADPH oxidase. In plants attacked by the biotype RWA1 there occurred differential expression of a greater number of genes than in the variant with RWA2 (biotype with a wider range of pathogenicity) (37, 38).
Aphids are always polymorphic and heterogonic: along with normal males and females laying overwintering eggs, they always develop from 1 to 10-20 or more generations of parthenogenetic females (39). Evolution of aphids was probably parallel to evolution of plants; from several similar generations of sexually reproducing individuals aphids proceeded to heterogonic alternation of bisexual and parthenogenetic propagation (40). Mass reproduction of parthenogenetic generations in spring and summer leads to a rapid population growth of aphids. In autumn, the amphigonic generation produces overwintering eggs – a source of genetic variability and survival. These adaptive mechanisms allowed aphids to inhabit the whole world, especially areas with a temperate climate. G.Kh. Shaposhnikov (41) believes that not only particular species, subspecies, races and biotypes, but even individual clones and even individuals differ by host specificity and degree of preference of the same host plants, as well as adaptivity to a new feed. Great plasticity of aphids has many reasons, among which is a long-term impact of variable living conditions, especially diet.
Genetic adaptation of aphids to host plants is a widespread and documented phenomenon. Intraspecific forms of aphids show differential interaction with host genotypes, and these biotypes express different capacity for overcoming the host resistance (42).
Genetic mechanisms of host-parasite relationship and their co-evolution were revealed by H. Flor, who studied genetic aspects of resistance of flax to rust fungus and the pathogenicity of Melampsora lini. According to the postulate “gene-for-gene”, for each resistance gene of a host there is a corresponding virulence gene of the parasite. Mutation in the pest’s virulence gene causes the loss of efficiency of the host’s resistance gene (43). In the view of H. Flor, resistance genes are usually dominant as evolutionarily more “old”, while virulence of a parasite (slave partner) is recessive. “Gene-for-gene” relationship has been demonstrated on a number of host-parasite pairs including S. graminum-wheat (42) and S. graminum-sorghum (44). Recently, such interactions have been confirmed by molecular studies.
Biological value of parasitic specialization and intraspecific differentiation of parasites was described by N.I. Vavilov in his  final work “The Laws of Natural Plant Immunity to Infectious Diseases” presented at the meeting of Biology Division of the USSR Academy of Sciences in 1940 and published posthumously in 1961. “The first and fundamental law which determines the existence of plant species and varieties resistant to a particular parasite, is specialization of parasites, their attachment to a specific range of hosts, species or genus of wild and cultivated plants. The phenomenon of specialization seems to be the major factor in evolution of parasitism... The more a parasite is specialized on certain host genera and species, the more is probable the occurrence of immune forms within individual species” (45).
Cereal aphids are oligophagous, they affect both cereals and other monocots (Juncaceae, Cyperaceae, Liliaceae) (39). Barley is usually the most preferred crop. Differential interaction with host plants has been described in detail for almost all economically most harmful aphid species: Schizaphis graminum(46), Diuraphis noxia (47), Rhopalosiphum maidis (48), Sitobion avenae (49) and Rhopalosiphum padi (50). Intraspecific variation has been thoroughly investigated in the most harmful species - S. graminum and D. noxia.
In Krasnodar population of S. graminum the long-term monitoring of genetic structure has revealed both general and seasonal polymorphism of its pathogenicity in respect to six sorghum samples with different resistance genes; totally, 42 virulence phenotypes (biotypes) of aphids have been identified, and from 18 to 36 per year. Abiotic factors can change relative competitiveness of aphid clones, which affects seasonal variation in occurrence of particular biotypes. Consequently, changes of environmental conditions lead to differentiated selection in population of S. graminum (51).
“The second fundamental law that determines the probability of occurrence of immune varieties and species within a particular crop is the presence or absence of a sharp genetic divergence... The most contrasting differences in immunity will distinguish the plants cytogenetically sharply differentiated to various species” (45). Discussing the situation, N.I. Vavilov mentioned such crops as wheat – a large number of diverse botanical species with pronounced variation of immunity to diseases, and barley – a narrower genetic group with smoothed differences.
The authors have studied 4527 samples of soft and durum wheat from different eco-geographical zones of the former Soviet Union in respect to their resistance to R. padi and S. avenae, and only 48 forms low-affected by aphids have been found among them. For R. padi, sufficiently high antibiosis (host’s counteraction to a feeding pest) was expressed by eight varieties of spring wheat. The gene pool of cultivated Triticum aestivum and T. durum has a relatively small number of resistant forms, so a promising way to obtain such forms is investigating wild wheat species suitable for introgressive breeding. Such studies suggest that the gene pool of Triticum is quite diverse by resistance to S. avenae. The best resistance have diploid species with genomes Au (T. urartu) and Ab (T. boeoticum, T. monococcum), D genome provides good resistance as well (T. kiharae and T. miguschovae), while the resistance associated with G genome is compromised as pests can overcome it (52).
The immunity of sorghum to S. graminum has been investigated in more than 5 thousand samples related to four economic groups (grain, sugar, broomcorn, grass) from all centers of crop formation, as well as in 110 wild samples. Highly resistant samples have been detected among cultivated species of grain sorghum and Sudan grass; their immunity to the pest is determined by 15 resistance genes, 10 of which – new-identified, not involved in breeding work earlier. At the same time, a differentiated interaction with the pest haven’t been detected only in the samples protected by Sgr7-Sgr11 genes, so it necessitates a further search for samples with new resistance genes. Another genetic feature of this plant genus is a frequent occurrence of weakly expressed resistance genes (53, 54).
Unfortunately, the genus Sorghum still has no generally accepted taxonomic classification – it has been described as one species, or several dozen species; taxa of many forms are undetermined. The forms most damaged by aphids are S. guineense, S. nervosum, S. caffrorum, S. nigricans, by economic groups – sugar sorghum is the most damaged, grain sorghum – somewhat less affected, then broomcorn and grassy sorghum. However, resistant samples have been found within each of these groups. It is known that all cultivated forms of sorghum hybridize with each other, and hybrids between cultivated and wild species are usually fertile. So, the authors assume that there’s no point to search for a close relationship between botanical species and pest resistance. Unlike wheat, for sorghum there’s no prospect for an introgression of resistance genes from wild species (53).
"The third major law of plant immunity is a correlation between immune response to parasitic diseases and ecological type of a plant. ... The most contrasting variations of immunity can be revealed ... in the most contrasting environmental conditions” (45).
The authors’ studies have proved the relationship between ecological type of plants and resistance to S. avenae. Thus, in T. dicoccum the infestation of ears was quite variable depending on geographical origin of a host sample. European (subsp. dicoccum) and Moroccan (subsp. maroccanum) samples  were not resistant to aphids. Moderately resistant samples were detected among Eastern (subsp. asiaticum) and Ethiopian (subsp. abyssinicum) forms: K-13635, K-13483, K-43872 (Armenia), K-6391 (Azerbaijan), K-14380 (Turkey ), K-19622 (Ethiopia), etc. T. monococcum can be considered as generally resistant to S. avenae, but in Dagestan there was observed a significant variation in this trait. The maximum damaged samples are the ones related to Western Europe and Mediterranean ecological groups: K-40063, K-41931, K-46746 (Germany), K-20498, and K-21038 (Italy) (52).
According to N.I. Vavilov, “... immunity is being developed through a natural selection only in those conditions that promote the infection, and, as a rule, it is usually expressed only in the presence of a particular parasite on which the immunity is focused” (45), which slightly disaccords with a later interpretation that immune forms can be found mainly in centers of a crop origin.
Sorghum forms resistant to S. graminumhave been found by the authors among the local samples from China, not from Africa (primary center of its origin), which fact can be associated with ancient relationship between the pest and the host plant. G.Kh. Shaposhnikov (41) believed that most of the aphids originate from one primary center in the mountains of Manchu-Chinese and Indian sub-areas. In experimental studies of barley and oats, many samples from South-East Asia have been proved as resistant to aphids. Among 490 samples of barley from China (mostly local forms) there have been identified 93 resistant to S. graminum. The highest rate of resistant barley forms was identified among the samples from China provinces of Shaanxi (47,1% of a total studied) and Shanxi (34,9%) (55). Among 277 samples of oats from Primorsky Krai, Mongolia, China and Japan there have been detected 85 forms with heterogeneous resistance to S. graminum. It was assumed that resistance properties of these samples are protected by genes distinct from those identified previously (56).
The fourth Vavilov’s law of natural immunity was confirmed by the author’s study as well: “... a groupwise, or complex, immunity is a quite real fact widespread in nature” (45). The evidence are T. monococcum samples with combined immunity to three aphid species: R. padi, S. avenae and S. graminum (52). The literature data suggest a complex resistance of T. monococcum to various pests and diseases: aphids, wheat thrips, sunn pest, frit flies, sawflies, cereal leaf beetle, mildew, smut fungi, rust fungi etc. (45, 57, 58). N.I. Vavilov noted T. monococcum as “an accumulator of a complex immunity”. Today, introgressive selection of wheat is one of the most effective ways to create new forms highly resistant to pests and diseases.
Upon the abovementioned laws N.I. Vavilov formulated the fifth and sixth laws. “Knowing the evolution of a crop, ... it can be largely predicted the location of immune forms important for a breeder” (45). “Ecological and geographical regularities in the expression of immunity can be relatively common, peculiar to various plants often related to different genera and even families. The development of susceptible or immune forms involves not only individual species or genera, but whole groups whose evolution occurred in the same territory”(45).
These regularities confirm the abovementioned facts about the resistance to S. graminum in sorghum, barley, and oats. Another example - the resistance to D. noxia most often found in wheat (59) and barley (60) forms originated from Central Asia and the region of Caspian Sea where this pest is an endemic species.
Practical aspects of Vavilov’s works prevailed in his own opinion: “The development of cereal varieties resistant to fungal diseases is one of the urgent tasks of plant breeding today. The first step to solve this problem is a detailed study of existing forms of cereal crops in respect to their relationship with parasitic fungi” (61). Knowing that resistant samples are rare, Vavilov emphasized the great importance of related species in the establishment of immune forms, as well as the role of mutagenesis in breeding for resistance.
The authors’ findings show that both major and minor genes of cereals’ resistance to aphids differentially interact with pests’ genotypes, so, there’s an obvious possibility of pest adaptation in both cases.
Thus, the presented concept of breeding cereal crops for resistance to aphids is based primarily on increasing the genetic diversity of cultivated varieties. This task can be achieved by different ways depending on the crop: e.g., in wheat - mainly through introgression, in sorghum – identification of resistant forms among cultivated species. The adaptation of pests to resistant varieties can be reduced through the expedient territorial distribution of donors with various resistance genes within a pest habitat. This approach requires the knowledge of genetic structure of pest populations, their diversity and interrelations, as well as the variation of pest pathogenicity in respect to host plants. However, the practice of “irregular” mosaic, i.e. not regulated joint growing of many varieties with different resistance genes, is quite possible at present.

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