Abstract
Worldwide, wheat (Triticum aestivum L.) is playing a significant role in meeting the global food security; however to cope up with the booming human population, pressure on natural resources is tremendously increasing to get higher crop yields. The crops are under continuous threat by several stresses (biotic and abiotic) and these are taking heavy toll on crop yields. Among the various biotic factors hampering wheat production, aphids are considered as a major biotic threat to food grain security because the pest causes both quantitative and qualitative losses. Eleven different aphid species are reported to attack wheat out of which, five species, viz., Rhopalosiphum padi, Rhopalosiphum maidis, Schizaphis graminum, Sitobion avenae and Diuraphis noxia, cause considerable economic damage to wheat crop. Aphids suck sap from tender plant parts and cause 20–30% yield losses in cereal crops. Apart from direct losses, aphids also inject toxins via saliva and transmits barley yellow dwarf virus. Because of short life span and high dispersal rates, aphid management is a challenging job and large amounts of pesticides are being used for their control in wheat. It leads to destruction of non-targeted beneficial natural enemies and problems of insecticide resistance and pest resurgence. Host plant resistance is considered as an eco-friendly approach and constitutes an integral component of IPM programmes. Breeding crops for insect-pest resistance have gained momentum over the past few years, and several insect-resistant crops have been developed. There is a tremendous scope of development of wheat genotypes having genes for durable insect resistance against aphids with the discovery of new molecular tools. The chapter will cover host plant resistance mechanism against aphids in wheat based on biochemical, genetic and physiological parameters and progress made towards identification of resistant donors. Besides, challenges in breeding wheat varieties for aphid resistance and potential of transgenic in aphid resistance programme are also discussed.
Access provided by Autonomous University of Puebla. Download chapter PDF
Similar content being viewed by others
Keywords
- Antibiosis
- Antixenosis
- Diuraphis noxia
- Genetic resources
- Pre-alighting response
- Resistant donors
- Transgenics
1 Introduction
Wheat is the most widely grown crop in the world and a staple food for 1/3rd population of the world. Wheat crop yields are affected by several abiotic and biotic stresses. Earlier wheat crop was considered as insect-pest-free crop but now due to input-intensive agricultural practices and changing climatic conditions; insect-pests have emerged as a serious inhibiting factor in cereal production. Amongst the various insect-pests, aphids are considered as one of the major biotic threats to production in wheat-growing regions of the world. Eleven aphid species are reported to attack wheat, out of which five species, viz., Rhopalosiphum maidis Fitch, Rhopalosiphum padi L., Schizaphis graminum (Rondani), Sitobion avenae Fabricius and Diuraphis noxia (Mordvilko), cause considerable economic damage to wheat crop (Deol et al. 1987). Aphids suck phloem sap from tender plant parts and secrete honey dew on which black sooty mould grows. This saprophytic fungus reduces the photosynthetic efficiency of plants (Rabbing et al. 1981). They cause 20–30% yield losses in cereal crops by direct feeding (Voss et al. 1997; Singh and Deol 2003). Apart from the direct damage by sucking sap from foliage, they also inject toxins via saliva and act as efficient vectors of barley yellow dwarf virus (Leather and Dixon 1984). Because of their short life span and high dispersal rates, aphid management is a challenging and their control in wheat primarily relies on pesticide treatments. The indiscriminate use of pesticides causes the significant reduction of non-targeted organisms including aphids’ natural enemies and chemical residue mobility to higher levels of the trophic chains, and it can also generate pest populations with insecticide resistance due to the strong selection pressure on the pest populations (Mitchell et al. 2017; Singh and Kaur 2017). Alternatively, host plant resistance to insects (HPR) is an eco-friendly and economically sound approach for farmers and a fundamental component of IPM programmes. It is defined as a set of plant heritable traits that reduce the damage caused by a pest compared with other plants of the same species which lacks these traits and are under the same pest pressure. The host plant resistance is governed by certain genes that express the presence or absence of certain morphological or biochemical traits that actually affect ability of an insect-pest to utilize the plant as a host.
Since the beginning of agriculture, the importance of varietal improvement is well known. In the ancient times, selection and introduction were commonly used methods, until the knowledge about hybridization, mutation and polyploidy emerged. Possibly, the earliest documented report on plant resistance to insects was the observations of Hessian fly on different wheat cultivars by farmers in the USA (Havens 1801). The first Hessian fly-resistant wheat (cv. Underhill) was cultivated by farmers in the eighteenth and nineteenth centuries. Snelling (1941) published the first review on the status of the knowledge of plant resistance to insects and reported that more than 90% of the HPR studies at the time were published between 1920 and 1941, despite that the first documents came to light in the nineteenth century. The first comprehensive review and conceptual framework of HPR to insects was established based on the work of Reginald H. Painter (1941). Despite the growing interest in HPR during early years of the twentieth century, the importance of HPR as one of the insect control methods remained under the shadow of chemical control after the World War II. Insecticides such as DDT showed spectacular results during post-World War II period and research strategies shifted from HPR to chemical control. However, Rachel Carson (1962) in her book The Silent Spring was the first to highlight the detrimental effects of pesticides to the environment and human beings. This book was important to again tilt the balance towards HPR and started the new era of modern environment-friendly methods of pest control.
Currently, breeding crops for pest resistance have gained momentum and some insect-resistant crops have been developed. With the advent and use of modern technologies, the field of plant resistance to arthropods offers enormous opportunities for the continuous development of crop cultivars carrying insect resistance genes. However, several challenges remain to be overcome. For instance, marker-assisted selection (MAS) can aid in developing varieties carrying resistance genes; however, identification of diagnostic markers is challenging. Another example is high-throughput phenotyping which can facilitate the evaluation of large population sizes; however, work on spectral signatures related to aphid damage in wheat remains limited. These new approaches developed in host plant resistance field will act as a solid interdisciplinary activity that will significantly improve the pest management practices and consequently increase food production in a sustainable way.
This chapter summarizes the information related to categories of host plant resistance, availability of genetic resources for aphid resistance in wheat, breeding/molecular techniques employed for introgression of aphid resistance in cultivated wheat and challenges and future prospects in aphid resistance programme.
2 Resistance Categories Against Aphids in Wheat
Painter (1941) classified host plant resistance to insects in three categories, i.e. non-preference, antibiosis and tolerance. Non-preference was later renamed to antixenosis to describe a plant characteristic rather than an insect response (Kogan and Ortman 1978). These categories are frequently found in combination, and it can be difficult to separate their individual effects in a resistant plant. This separation into categories is useful to determine evaluation procedures and further investigate the mechanisms underlying the resistance. Authors, however, have proposed a modification of Painter’s concept of HPR to insects, based on the complexity of separating the actual causes for antibiosis and antixenosis (Stout 2013; Stenberg and Muola 2017). Even though the discussion of the conceptual framework is not within the scope of this chapter, we consider that the traditional definition (Smith 2005) is valid for measuring the resistance, as it reflects categories of the resistance and not the actual causes and mechanisms as some references in the scientific literature tend to confuse or use indistinctly.
Host plant resistance affects the host selection process in aphids, which can be divided in six stages: (a) pre-alighting behaviour, (b) assessment of surface cues before stylet insertion, (c) probing epidermis, (d) stylet pathway activity, (e) sieve element puncture and salivation and (f) phloem acceptance and sustained ingestion (Powell et al. 2006). Host plant resistance operates during this process by exhibiting any of the three categories of resistance by means of different resistance mechanisms.
2.1 Non-preference/Antixenosis
It mainly affects the pest’s behaviour and is considered as the first line of defense in plants against insect damage. Antixenotic traits make the plants less suitable for insect/aphid colonization and adversely affect their host finding ability. The host finding process in insects consists of pre- and post-alighting phases and involves olfactory, visual, gustatory and thigmotactic responses (Smith 2005). Host selection in aphids is predominantly governed by chemical cues (Powell and Hardie 2001), but at the same time, visual signals also play a significant role in host finding process (Doering and Chittka 2007).
2.1.1 Pre-alighting Responses
Visual cues: Visual cues during host searching process depend upon the spectral quality of light and colour, size, shape and dimensions of the plants (Smith 2005). The aphids usually prefer yellow-coloured surfaces (Pettersson et al. 2007). However, R. padi has higher attractiveness to green than yellow colour as compared to other aphid species infesting wheat crop (Kieckhefer et al. 1976). The size of the green/yellow-coloured area (plant density) is another important factor which determines the landing rate of aphids on plant (Ahman et al. 1985). Moharramipour et al. (1997) also reported that yellow and non-waxy leaves of barley are preferred by cereal aphids for feeding or have additive effect on aphid resistance. The co-evolution theory of colour preference on Prunus padus L. also revealed strong preference of R. padi towards green leaves (Archetti and Leather 2005).
Olfactory cues: The volatiles released by plants can act as repellents or attractants to insects. These volatiles are received by primary olfactory structures of insects located in last two segments of the insect antennae (Gillot 2005). Many volatiles are common to all plants, whereas some of these are specific to certain plant genera or species or cultivars/varieties (Bruce et al. 2005). In few cases, only upon insect damage, some volatiles are released by the plants. Methyl salicylate and cis-jasmone are such compounds released by plants during aphid feeding and act as repellent to the R. padi, S. avenae, S. miscanthi (Takahashi) and Metopolophium dirhodum (Walker) (Hardie et al. 1994; Pettersson et al. 1994; Birkett et al. 2000; Pickett and Glinwood 2007). The direct spraying of these compounds on wheat plants at seedling stage exhibited negative effects on aphid growth and positive effects on some natural enemies such as ladybird beetles and parasitoids (Birkett et al. 2000; Bruce et al. 2003).
2.1.2 Post-alighting Response
The aphid behaviour after landing on the plants is further influenced by a wide range of characters associated with plant morphology and chemistry (Pettersson et al. 2007). After stylet insertion into a particular host plant, aphids make the decision to reject or accept it as host or not (Powell et al. 2006). Aphids are reported to suck sap in small quantities and then these samples are rapidly transported to the pharyngeal organ. Aphid penetration process into the host is divided into three stages: (1) pathway stage, the stage where brief cell punctures occur; (2) xylem stage, drinking stage to relieve water stress; and (3) phloem stage: where the main feeding takes place. The final decision to accept or reject a plant is made at the phloem level (Pettersson et al. 2007). Significant differences have reported in literature about the feeding behaviour of aphids on resistant versus susceptible wheat genotypes (Pereira et al. 2010; Greenslade et al. 2016; Singh et al. 2020).
Antixenosis tests measure the differential response of insects among different plant genotypes. It can be expressed as the relative amount of feeding or oviposition among different genotypes. Free-choice test is the most common type for checking antixenosis in aphids. In this test, firstly, each genotype is equidistantly placed in a circular pattern and then aphids are released in the centre of the circle, and then counts of aphids feeding/oviposition are made after a particular interval of time (Webster et al. 1994; Hesler et al. 1999; Hesler 2005). Leaf discs from different plant genotypes can also be placed in glass vials with distilled water and held in a testing platform as a slight modification in this free-choice test. Nowadays, the volatiles collected from the plants are placed on the different arms of olfactometer for antixenosis tests (De Zutter et al. 2012). One important aspect to be considered while carrying out such studies is light orientation. The orientation of light must need to be managed properly as aphids are attracted to light sources, and it may lead to false resistance/susceptibility response. Antixenosis reduces the initial infestation and can be considered as an important component of host plant resistance. However, importance of antixenosis decreases in the current agricultural systems where monoculture predominates and deprives the pest of its preferred host and eventually it starts accepting a less preferred host.
2.2 Antibiosis
This category negatively affects the physiology of an insect. As a result of antibiosis, higher mortality, smaller body size/weight, reduced fecundity or prolonged periods of insect development can be observed (Smith 2005). This type of resistance against aphids has been found in several wheat and barley genotypes (Hesler et al. 1999; Hesler 2005; Aradottir et al. 2016; Singh et al. 2020). In this type of resistance mechanism, the allele chemicals or non-nutritional chemicals produced by the plants usually affect the biology or behaviour of aphids. Givovich and Niemeyer (1996) reported that hydroxamic acid present in some wheat genotypes adversely affects the biology of D. noxia. The two genes Dn5 and Dn1 conferring antibiosis to this species were reported to be related to concentrations of secondary metabolites (Ni and Quisenberry 2000). However, Macaulay et al. (2020) reported that QTL for gramine content is not linked to aphid resistance in barley.
Changes in host plant chemistry and increased nutritional status of plants have been observed in aphid-infested plants (Telang et al. 1999). The increased concentration of essential amino acids in infested plants was reported upon feeding by nymphs of D. noxia. Similarly, Castro et al. (2007) reported significant increases in protein content in S. graminum-infested wheat plants. Although, antibiotic effects are mainly observed by biochemical profiles of plants, however plant structures like trichomes can have direct negative effect on the physiology of insects.
Host plant resistance mechanism studies revealed that methodologies for identifying antibiotic effects are more strenuous than antixenosis tests since information related to relative development, reproduction and mortality of insects on different plant genotypes is required. Life tables consisting of data about insect longevity, mortality, fecundity and intrinsic rate of increase (rm) on different genotypes need to be developed for such studies. But time is required to do life table studies; therefore alternative techniques involving aphid fecundity and rm, such as mean relative growth rate (MRGR) and relative growth, can be used for aphid screening purpose (Leather and Dixon 1984; Cheung et al. 2010).
2.3 Tolerance
Tolerance is defined as the ability of plants to withstand or recover from an insect attack equal to the attack caused in a susceptible genotype. It is determined by the genetic characteristics that enable plants to continue growing, recover or add new growth after and/or during insect damage (Smith 2005). It has been observed that tolerant plants tend to produce more biomass and involve plant traits related to biomass production. Rosenthal and Kotanen (1994) reported that compensation, seen as regrowth, depends upon the storage capacity, photosynthetic rate, allocation patterns and nutrient uptake of plants. These traits may change under varying external (environment, insect species and spatial distribution) and intrinsic (plant genetics) factors. Tolerance phenomenon has been widely reported, and it is known to be frequently interacting with the other mechanisms of resistance. For example, in wheat and barley, tolerance to aphids has been reported by several authors (Hesler et al. 1999; Smith and Starkey 2003; Lage et al. 2004; Hesler 2005; Zhu et al. 2005). It has been reported that Russian wheat aphid (RWA)-tolerant plants often possess higher photosynthetic rates and resulted in higher growth rates and stored root carbon (Heng-Moss et al. 2003). The foliage of aphid-tolerant plants have highly expressed photosystem and chlorophyll genes associated with photosynthesis (Marimuthu and Smith 2012). Boyko et al. (2006) suggested that the molecular basis for tolerance to D. noxia in plants carrying the Dnx gene involves the up-regulation of transcription sequences similar to those that regulate photosynthesis, photorespiration, protein synthesis, antioxidant production and detoxification. Ni et al. (2002) showed that non-damaged leaf areas of plants infested with D. noxia increased their concentrations of chlorophylls and help the plants to compensate the loss of photosynthetic capacity by increasing metabolic activity in non-damaged areas.
Tolerance mechanism is cited as advantageous as it does not pose any selection pressure on the pest populations; therefore it is expected that this type of resistance is more durable than antixenosis and antibiosis. Though, it is a complex mechanism that ultimately influences plant biomass production and yield.
The measurement of tolerance mechanism is dependent on the aphid species that is being evaluated as it is related to the plant responses to insect damage. Estimating chlorophyll loss is also an indicative of the tolerance response against D. noxia and S. graminum (Lage et al. 2003, 2004; Sotelo et al. 2009). Tolerance studies using plant growth and biomass measurements after exposure of genotypes for a certain period can also be alternatively used (Hesler et al. 1999; Hesler 2005; Dunn et al. 2007).
3 Breeding for Aphid Resistance
Host plant resistance is an economical and ecologically sound strategy and constitutes a fundamental component in any IPM (integrated pest management) programme. The first step for successful aphid breeding programme is the identification of adequate levels of resistance in the wheat gene pool. Wild relatives of wheat and landraces are the most important potential sources for aphid resistance. The possibility of finding good aphid resistance sources is always bright if the germplasm is selected from the aphids’ centre of origin or where the wild relatives/landraces have historically co-evolved with the aphids.
3.1 Identification of Resistant Donors
Correct identification of resistant donors is the most important step for aphid resistance breeding programme. The screening methods for identification of sources of resistance should be based on the symptoms of attack and biology/behaviour of aphids. Several protocols have been developed to screen the germplasm and identify resistant genotypes against aphids in wheat (Berzonsky et al. 2003; Anonymous 2004; Dunn et al. 2007). The chlorophyll content can be used as an indirect method (tolerance) for identification of resistant germplasm to aphid species that cause chlorosis, such as S. graminum and D. noxia (Franzen et al. 2008). Some methods to measure antibiosis and antixenosis are already discussed in the earlier section and can be used to screen germplasm or segregating populations under field/laboratory conditions. However, assessing antibiosis generally laborious and time-consuming.
Frequently, all three categories of resistance are present in a single plant genotype, and it becomes difficult to distinguish if reduced performance of aphids is due to antibiotic or antixenotic effects. The techniques including a combination of different resistance mechanisms should be used for identification of resistant germplasm. Another consideration for wheat breeding is the genetic diversity of aphid population. One should consider the target region/area for which wheat is bred and have information related to the aphid dynamics and prevalent aphid biotypes of the region.
3.1.1 Available Genetic Resources for Resistance to Aphids in Wheat
The polyploid nature of wheat allows introgression of genes from related species. The selection of breeding method for introgression of genetic resistance from related species in wheat depends upon the evolutionary distance between the species (Friebe et al. 1996). The resistance from primary gene pool (Triticum turgidum L., Triticum dicoccoides L., Triticum monococcum L. and Aegilops tauschii Coss.) can be attained by direct hybridization, homologous recombination and backcrossing; however, homologous recombination can be used for transferring resistance from the secondary gene pool (polyploid Aegilops species, Secale species, Thinopyrum elongatum (Podp.), Thinopyrum intermedium (Host)). Transfer of resistance from tertiary gene pool is little hard, but still techniques such as centric breakage fusion of univalents, induced homoeology and radiation treatment to induce chromosome breaks may be used to transfer resistance from tertiary pool (Friebe et al. 1996).
Resistance to S. graminum has been found in chromosome 1R of rye and 7D of Ae. tauschii (Kim et al. 2004; Mater et al. 2004; Zhu et al. 2005; Lu et al. 2010). Similarly, S. avenae, D. noxia and R. padi resistance has been found in rye, Aegilops species (Crespo-Herrera et al. 2013, 2019a, b) and Triticum araraticum Jakubz (Smith et al. 2004). Ploidy level plays an important role in resistance to aphids, and genotypes with low ploidy level were more frequently resistant to aphids (Migui and Lamb 2003). In general, Triticum boeoticum Boiss., Ae. tauschii and T. araraticum had the higher levels of antibiosis to R. padi, whereas Ae. tauschii and T. turgidum had the higher levels of overall resistance to S. graminum, whereas T. araraticum and T. dicoccoides presented the higher levels of overall resistance to S. avenae (Migui and Lamb 2003). Singh et al. (2006) and Singh and Singh (2009) also identified confirmed sources of R. maidis resistance in barley. Genetic resources of resistance to certain aphid species in wheat and wheat-related species are discussed below:
3.1.1.1 Bird Cherry-Oat Aphid (Rhopalosiphum padi)
The origin of this aphid species is difficult to trace because it is currently distributed worldwide and its sexual phase takes part on various Prunus species (Blackman and Eastop 2007). This aphid species can reduce yield by 31–62% (Voss et al. 1997; Riedell et al. 2003). A. elongatum, A. intermedium, A. repens and Elymus angustus and their introgression wheat lines were first found to show antibiotic type of resistance (Tremblay et al. 1989). Resistance has also been found in wheat-rye translocation lines, and triticale was identified which possesses all three categories of resistance to R. padi (Hesler 2005; Hesler and Tharp 2005; Hesler et al. 2007; Crespo-Herrera et al. 2013). Recently, Singh et al. (2018) identified R. padi resistance in some Ae. tauschii lines. Quantitative trait loci conferring tolerance and antibiosis have been mapped in synthetic-hexaploid wheat (Crespo-Herrera et al. 2014). However, resistance to R. padi has not been purposely incorporated into elite wheat cultivars (Porter et al. 2009).
3.1.1.2 English Grain Aphid (Sitobion avenae)
This aphid originates in Europe and currently it is distributed in Africa, India, Nepal, North America and South America (Blackman and Eastop 2007). Normally populations of S. avenae have highest reproductive rate at heading stage and cause 3–21% yield losses in spring by feeding at booting stage (Watt 1979; Voss et al. 1997; Singh and Deol 2003). However, the damage caused by the S. avenae is less deleterious than S. graminum and R. padi at the same population density (Kieckhefer and Kantack 1980; Voss et al. 1997). So far only one resistance gene (RA-1 located on 6AL chromosome) linked to EGA resistance has been mapped in the durum wheat line C273. This gene is reported to be linked to SSR markers Xwmc179, Xwmc553 and Xwmc201 (Liu et al. 2011). Resistance to S. avenae has been also identified in some wheat-rye translocation lines and wheat relatives such as T. monococcum, T. boeticum, T. araraticum, T. dicoccoides and T. urartu (Di Pietro et al. 1998; Migui and Lamb 2003, 2004; Crespo-Herrera et al. 2013).
3.1.1.3 Greenbug (Schizaphis graminum)
This species is widely distributed in Asia, Southern Europe, Africa and North and South America (Blackman and Eastop 2007) and can cause 35–40% damage to winter wheat (Kieckhefer and Gellner 1992). The first resistance gene (Gb1), conferring resistance to S. graminum biotypes A, F and J, reported was in ‘DS28A’, which is a hexaploid selection from the durum wheat Dickinson (Curtis et al. 1960; Porter et al. 1997). However, biotype ‘B’ of GB developed the ability to damage S. graminum-resistant DS28A genotype in 1961 (Porter et al. 1997). Since these different S. graminum populations were designated according to their capability to injure plant genotypes with certain resistance genes, the ‘biotype’ concept is related to a phenotypic expression that does not totally reflect aphid genetic diversity (Blackman and Eastop 2007). Weng et al. (2010) found that biotypes E, I and K are genetically related, whereas biotype H is genetically distant from all of the other biotypes. Host association may have a significant role in this genetic differentiation, since different biotypes were found on different hosts, viz., I and K biotypes were first identified in sorghum, biotype E was first identified in wheat, biotype G on Agropyron species and biotype H on Ae. cylindrica and A. intermedium (Burd and Porter 2006; Weng et al. 2010). Several S. graminum biotypes have been identified and known to be present in nature before the deployment of resistance genes (Porter et al. 1997; Berzonsky et al. 2003). Various S. graminum resistance genes (Gb1, Gb2, Gb3, Gb4, Gb5, Gb6, Gb7/Gbx2, Gb8, Gba, Gbb, Gbc, Gbd, GbSkl, Gbx1, Gby and Gbz) are reported in wheat (Burd and Porter 2006; Crespo-Herrera et al. 2019a, b; Xu et al. 2020) and related plant species originating mostly from Ae. tauschii. Genes Gba, Gbb, Gbc, Gbd and Gbx1 are located in the same region of chromosome 7D and linked to Xgwm671 SSR marker (Zhu et al. 2005). All these genes (except Gbx1) are either allelic or linked (Zhu et al. 2005). SSR markers Xbcd98 and Xwmc157 are tightly linked to Gby and Gbz genes, respectively. These Gby and Gbz genes are located on chromosomes 7A and 7D, respectively (Zhu et al. 2004; Boyko et al. 2006).
3.1.1.4 Russian Wheat Aphid (Diuraphis noxia)
Genes identified against different aphid species are listed in Table 16.1. This aphid species injects a toxin into plants while feeding resulting in a characteristic leaf rolling symptoms; however feeding at the earhead stage results in bending of earheads (Blackman and Eastop 2007). It is distributed in East Asia, South Africa, Australia and North and South America, but not reported in India and adjoining countries. D. noxia can cause up to 40% yield losses in winter wheat (Kieckhefer and Gellner 1992; Yazdani et al. 2017). Currently, 13 genes are catalogued to confer resistance to D. noxia, designated from Dn1 to Dn9, Dnx, Dn2401, Dn626580 and Dn1881, but other marker trait associations have been reported (McIntosh et al. 2013; Joukhadar et al. 2013). All these single dominant genes except for Dn3 are recessive, and most of them are located in the D genome except one in the B genome and another one in 1RS from rye. Liu et al. (2011) showed that Dn1, Dn2 and Dn5 resistance genes (located on 7DS) are either allelic or tightly linked to one another. All these genes are linked to the same SSR marker Xgwm111 (Liu et al. 2011). Unlike the development of S. graminum biotypes, it is believed that the occurrence of new genetic variation in D. noxia with the ability to harm wheat is due to the deployment of resistant cultivars (Weiland et al. 2008). Until 2003, only one biotype was reported in the USA; however, Haley et al. (2004) identified a new biotype RWA-2, and Dn7 gene from rye was found to be effective against this aphid biotype (Haley et al. 2004). In 2006, three new RWA biotypes were identified, RWA-3, RWA-4 and RWA-5, of which RWA-3 is virulent to all known resistance sources, including Dn7 (Burd et al. 2006). Weiland et al. (2008) identified three more biotypes in Colorado State, RWA-6, RWA-7 and RWA-8, to which Dn7 gene and the wheat genotypes Stars 02RWA2414-11, CO03765 and CI2410 are resistant.
4 Challenges in Breeding for Aphid Resistance
The main challenges to breed for aphid resistance in wheat as an additional component in breeding programmes are mainly: (1) accurate identification of resistance levels conferring the sufficient protection levels in the field, (2) to make breeding efficient, it is important to understand the genetics of the resistance and (3) the development of cost-effective selection tools that allow the accurate identification of resistant germplasm in breeding materials.
Presently most of the identified resistant genes wheat in with aphids in a gene for gene fashion, and deploying genes that confer resistance to more than one species would be the most ideal scenario, however, difficult to achieve. Hence, combining resistance genes is a suitable option in the absence of resistance genes with broad effects. But a careful selection of genes to be combined is crucial (Porter et al. 2000).
The presence of two or more aphid species on the same plant or in the same field is commonly observed. Under such conditions, there is competition between the two species for resources and usually one species predominates over the others. Therefore, growing resistant varieties to a single species repetitively may lead to the predominance of the species that was not previously problematic. The most desirable solution in such case is finding genetic resources resistant to multiple species is but not many sources are available in adapted germplasm; hence efforts are required to transfer the resistance from related species. Resistance to two or three aphid species have been found in wild relatives of wheat. Deciphering the genetic basis of such resistance sources is important, since the number of genes and their interactions are important aspects for plant breeding procedures.
One of the challenges for big breeding programmes is that protocols to evaluate aphid resistance are difficult to implement on a large scale, since the evaluation for aphids is highly time-consuming and labour intensive, even under controlled conditions. Selection for resistance to S. graminum and D. noxia, however, could be relatively easier compared with R. padi and S. avenae, since the former two species give typical plant symptoms that can be scored.
Another potential problem that has been observed is that sometimes there is no correlation between seedling and adult plant resistance and it also varies from one aphid to another species, for instance, as observed in case for S. avenae (Migui and Lamb 2004; Crespo-Herrera et al. 2013). Thus, screening techniques and phenotypic selection should be employed at both early and late plant stages. For development of high-yielding germplasm with resistance to quantitatively inherited traits, the combination of the selected bulk and single backcrossing approaches for wheat breeding has showed to be a highly effective strategy (Singh and Trethowan 2007). However, newer breeding strategies can be explored as well, such as the combination of rapid generation advancement with performance prediction aided by the utilization of molecular markers and advanced statistical procedures. Marker-assisted selection could facilitate plant selection during the breeding process. However, for this it is important to study the genetics of the resistance, identify the markers and develop those that are user-friendly. Some of the general considerations for wheat breeding involving quantitative traits suggested by Singh and Trethowan (2007) are the following:
-
(a)
Selection of parents: Proper care should be taken while choosing parents for crossing. Weightage should be given to breeding values as well as phenotypic information. It has been observed some genotypes have better combining ability as compared to others; therefore, such genotypes can inherit characters more easily to their offspring.
-
(b)
Crossing methodology: The approach of single backcrossing favours retention of most of the desired additive genes and thus allows incorporation and selection of useful small effect genes from the donor parents. This strategy has found to be more efficient for product development in breeding programmes. The parents used for crossing carrying different sets of additive genes should be favoured.
-
(c)
Size of population: Large populations of segregating material should be developed to increase the probability of selecting good combinations. Analysis of obtained lines with molecular tools should be done to confirm the presence of desired genes.
Additionally, Singh and Trethowan (2007) suggested that intercrossing the resistance sources before crossing them with the elite material should be carried out if broad resistance is not present in single plant genotypes. Besides having large segregating populations and utilizing flanking markers in early generations, it is possible to combine different resistance genes in single genotypes. This strategy could be carried out if multiple resistances to aphids are not found in single wheat genotypes.
5 Potential of Transgenic in Aphid Resistance Programme
Insect pheromones also offer potential for management of aphids in wheat. Bruce et al. (2015) first developed transgenic wheat by deploying the genes responsible for the biosynthesis of alarm pheromones, (E )-β-farnesene (Eβf), in the crop. It was achieved by using a synthetic gene based on a sequence from peppermint with a plastid targeting amino acid sequence, with or without a gene for biosynthesis of the precursor farnesyl diphosphate. In laboratory behavioural assays with these transgenic wheat plants, three cereal aphid species were repelled while foraging of a parasitic natural enemy. Although, these studies show considerable potential for aphid control, field trials employing the single and double constructs showed no reduction in aphids or increase in parasitism of natural enemies. Apart from social acceptance in public, the impacts of climatic conditions, insect density and inter- and intra-specific competition need further investigations for success of transgenic technology in wheat.
6 Conclusion and Future Prospects
The key component for getting success in resistance breeding against aphids is the exploitation of the large variation of resistance traits that exist in wild wheat relatives and landraces. To achieve this, the pre-breeding plays an important role in identification of potential resistant sources before transferring resistance from less adapted germplasm. Breeding for aphid resistance would be more feasible when it is exclusively targeted. However, this is usually not the case, and aphid resistance is considered as only one among several desired characteristics for its incorporation into cultivated wheat such as grain yield, yield stability, disease resistance, improved nutritional and end-use quality. Hence, initiatives should be taken to develop methods to easily implement aphid resistance in wheat breeding programmes, without sacrificing efficiency of breeding for other traits. There is no doubt that germplasm phenotyping for aphid resistance can be challenging; however it can be well-fitted and incorporated in breeding programme through current and new wheat breeding methods and technologies such as marker-assisted selection or genomic selection or RNAi.
References
Ahman I, Weibull J, Pettersson J (1985) The role of plant size and plant density for host finding in Rhopalosiphum padi (L.) (Hem.: Aphididae). Swed J Agric Res 15(1):19–24
Anonymous (2004) Progress Report of All India Coordinated Wheat and Barley Improvement Project 2004-05. Project Director’s Report. pp 1–66
Aradottir GI, Martin JL, Clark SJ, Pickett JA, Smart LE (2016) Searching for wheat resistance to aphids and wheat bulb fly in the historical Watkins and Gediflux wheat collections. Ann Appl Biol 70:179–188. https://doi.org/10.1111/aab.12326
Archetti M, Leather SR (2005) A test of the co-evolution theory of autumn colours: colour preference of Rhopalosiphum padi on Prunus padus. Oikos 110:339–343. https://doi.org/10.1111/j.0030-1299.2005.13656.x
Berzonsky WA, Ding H, Haley SD, Harris MO, Lamb RJ, McKenzie RIH, Ohm HW, Patterson FL, Peairs FB, Porter DR, Ratcliffe RH, Shanower TG (2003) Breeding wheat for resistance to insects. Plant Breed Rev 22:221–296
Birkett MA, Campbell CAM, Chamberlain K, Guerrieri E, Hick AJ, Martin JL, Matthes M, Napier JA, Pettersson J, Pickett JA, Poppy GM, Pow EM, Pye BJ, Smart LE, Wadhams GH, Wadhams LJ, Woodcock CM (2000) New roles for cis-jasmone as an insect semiochemical and in plant defense. Proc Natl Acad Sci U S A 97(16):9329–9334. https://doi.org/10.1073/pnas.160241697
Blackman RL, Eastop VF (2007) Taxonomic issues. In: Van Emden HF et al (eds) Aphids as crop pests. CABI, Wallingford, pp 1–29
Boyko E, Starkey S, Smith M (2004) Molecular genetic mapping of Gby, a new greenbug resistance gene in bread wheat. Theor Appl Genet 109(6):1230–1236. https://doi.org/10.1007/s00122-004-1729-2
Boyko EV, Smith CM, Thara VK, Bruno JM, Deng Y, Starkey SR, Klaahsen DL (2006) Molecular basis of plant gene expression during aphid invasion: wheat Pto-and Pti-like sequences are involved in interactions between wheat and Russian wheat aphid (Homoptera: Aphididae). J Econ Entomol 99(4):1430–1445. https://doi.org/10.1093/jee/99.4.1430
Bruce TJA, Martin JL, Pickett JA, Pye BJ, Smart LE, Wadhams LJ (2003) cisJasmone treatment induces resistance in wheat plants against the grain aphid, Sitobion avenae (Fabricius) (Homoptera: Aphididae). Pest Manag Sci 59(9):1031–1036. https://doi.org/10.1002/ps.730
Bruce TJA, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends Plant Sci 10(6):269–274. https://doi.org/10.1016/j.tplants.2005.04.003
Bruce TJA, Aradottir GI, Smart LE, Martin JL, Caulfield JC, Doherty A, Sparks CA, Woodcock CM, Birkett MA, Napier JA, Jones HD, Pickett JA (2015) The first crop plant genetically engineered to release an insect pheromone for defense. Sci Rep 5:118–112. https://doi.org/10.1038/srep11183
Burd JD, Porter DR (2006) Biotypic diversity in greenbug (Hemiptera: Aphididae): characterizing new virulence and host associations. J Econ Entomol 99(3):959–965. https://doi.org/10.1093/jee/99.3.959
Burd JD, Porter DR, Puterka GJ, Haley SD, Peairs FB (2006) Biotypic variation among north American Russian wheat aphid (Homoptera: Aphididae) populations. J Econ Entomol 99(5):1862–1866. https://doi.org/10.1093/jee/99.5.1862
Carson R (1962) The silent spring, 4th edn. Mariner Books, New York
Castro AM, Clua AA, Gimenez DO, Tocho E, Tacaliti MS, Collado M, Worland A, Bottini R, Snape JW (2007) Genetic resistance to greenbug is expressed with higher contents of proteins and non-structural carbohydrates in wheat substitution lines. In: Buck HTNJESN (ed) Wheat production in stressed environments. Springer, Dordrecht, pp 139–147
Cheung WY, Di Giorgio L, Ahman I (2010) Mapping resistance to the bird cherry-oat aphid (Rhopalosiphum padi) in barley. Plant Breed 129:637–646. https://doi.org/10.1111/j.1439-0523.2010.01771.x
Collins MB, Haley SD, Randolph TL, Peairs FB, Rudolph JB (2005) Comparison of Dn4 and Dn7 carrying spring wheat genotypes artificially infested with Russian wheat aphid (Homoptera: Aphididae) biotype 1. J Econ Entomol 98:16981703. https://doi.org/10.1093/jee/98.5.1698
Crespo-Herrera LA, Smith CM, Singh RP, Åhman I (2013) Resistance to multiple cereal aphids in wheat–alien substitution and translocation lines. Arthropod Plant Interact 7:535–545. https://doi.org/10.1007/s11829-013-9267-y
Crespo-Herrera LAA, Akhunov E, Garkava-Gustavsson L et al (2014) Mapping resistance to the bird cherry-oat aphid and the greenbug in wheat using sequence-based genotyping. Theor Appl Genet 127:1963–1973. https://doi.org/10.1007/s00122-014-2352-5
Crespo-Herrera L, Singh RP, Reynolds M, Huerta-Espino J (2019a) Genetics of greenbug resistance in synthetic hexaploid wheat derived germplasm. Front Plant Sci 10:782. https://doi.org/10.3389/fpls.2019.00782
Crespo-Herrera LA, Singh RP, Sabraoui A, El-Bouhssini M (2019b) Resistance to insect pests in wheat—rye and Aegilops speltoides Tausch translocation and substitution lines. Euphytica 215:123. https://doi.org/10.1007/s10681-019-2449-7
Curtis BC, Schlehuber AM, Wood EA Jr (1960) Genetics of greenbug (Toxoptera graminum (Rond.)) resistance in two strains of common wheat. Agron J 52:599–602. https://doi.org/10.2134/agronj1960.00021962005200100016x
De Zutter N, Audenaert K, Haesaert G, Smagghe G (2012) Preference of cereal aphids for different varieties of winter wheat. Arthropod Plant Interact 6(3):345–350. https://doi.org/10.1007/s11829-012-9184-5
Deol GS, Gill KS, Brar JS (1987) Aphid out break on wheat and barley in Punjab. Newslett Aphid Soc India 6:7–9
Di Pietro JP, Caillaud CM, Chaubet B, Pierre JS, Trottet M (1998) Variation in resistance to the grain aphid, Sitobion avenae (Sternorhynca: Aphididae), among diploid wheat genotypes: multivariate analysis of agronomic data. Plant Breed 117(5):407–412. https://doi.org/10.1111/j.1439-0523.1998.tb01964.x
Doering TF, Chittka L (2007) Visual ecology of aphids-a critical review on the role of colours in host finding. Arthropod Plant Interact 1(1):3–16
Dunn BL, Carver BF, Baker CA, Porter DR (2007) Rapid phenotypic assessment of bird cherry-oat aphid resistance in winter wheat. Plant Breed 126(3):240–243. https://doi.org/10.1111/j.1439-0523.2007.01345.x
Franzen LD, Gutsche AR, Heng-Moss TM, Higley LG, Macedo TB (2008) Physiological responses of wheat and barley to Russian wheat aphid, Diuraphis noxia (Mordvilko) and bird cherry-oat aphid, Rhopalosiphum padi (L.) (Hemiptera: Aphididae). Arthropod Plant Interact 2(4):227–235. https://doi.org/10.1007/s11829-008-9048-1
Friebe B, Jiang J, Raupp WJ, McIntosh RA, Gill BS (1996) Characterization of wheat-alien translocations conferring resistance to diseases and pests: current status. Euphytica 91(1):59–87. https://doi.org/10.1007/BF00035277
Gillot C (2005) Entomology. Springer, Dordrecht
Givovich A, Niemeyer HM (1996) Role of hydroxamic acids in the resistance of wheat to the Russian wheat aphid, Diuraphis noxia (Mordvilko) (Hom, Aphididae). J Appl Entomol 120(9):537–539. https://doi.org/10.1111/j.1439-0418.1996.tb01648.x
Greenslade AFC, Ward JL, Martin JL, Corol DI, Clark SJ, Smart LE, Aradottir GI (2016) Triticum monococcum lines with distinct metabolic phenotypes and phloem-based partial resistance to the bird cherry–oat aphid Rhopalosiphum padi. Ann Appl Biol 168(3):435–449. https://doi.org/10.1111/aab.12274
Haley SD, Peairs FB, Walker CB, Rudolph JB, Randolph TL (2004) Occurrence of a new Russian wheat aphid biotype in Colorado. Crop Sci 44(5):1589–1592. https://doi.org/10.2135/cropsci2004.1589
Hardie J, Isaacs R, Pickett JA, Wadhams LJ, Woodcock CM (1994) Methyl salicylate and (-)-(1RS,5S)-Myrtenal are plant–derived repellents for black bean aphid, Aphis fabe Scop. (Homoptera, Aphididae). J Chem Ecol 20(11):2847–2855. https://doi.org/10.1007/BF02098393
Havens JN (1801) Observations on the hessian fly. In: Charles R et al (eds) Transactions of the society for the promotion of agriculture, arts and manufactures, 2nd edn, New York, pp 71–86
Heng-Moss T, Ni X, Macedo T, Markwell JP, Baxendale FP, Quisenberry S, Tolmay V (2003) Comparison of chlorophyll and carotenoid concentrations among 30 Russian wheat aphid (Homoptera: Aphididae)-infested wheat isolines. J Econ Entomol 96(2):475–481. https://doi.org/10.1093/jee/96.2.475
Hesler LS (2005) Resistance to Rhopalosiphum padi (Homoptera : Aphididae) in three triticale accessions. J Econ Entomol 98(2):603–610. https://doi.org/10.1093/jee/98.2.603
Hesler LS, Tharp CI (2005) Antibiosis and antixenosis to Rhopalosiphum padi among triticale accessions. Euphytica 143(1–2):153–160. https://doi.org/10.1007/s10681-005-3060-7; https://doi.org/10.1007/BF02084437
Hesler LS, Riedell WE, Kieckhefer RW, Haley SD, Collins RD (1999) Resistance to Rhopalosiphum padi (Homoptera: Aphididae) in wheat germplasm accessions. J Econ Entomol 92(5):1234–1238. https://doi.org/10.1093/jee/92.5.1234
Hesler LS, Haley SD, Nkongolo KK, Peairs FB (2007) Resistance to Rhopalosiphum padi (Homoptera : Aphididae) in triticale and triticale-derived wheat lines resistant to Diuraphis noxia (Homoptera : Aphididae). J Entomol Sci 42(2):217–227. https://doi.org/10.18474/0749-8004-42.2.217
Joukhadar R, El-Bouhssini M, Jighly A, Ogbonnaya FC (2013) Genome-wide association mapping for five major pest resistances in wheat. Mol Breed 32:943–960. https://doi.org/10.1007/s11032-013-9924-y
Kieckhefer RW, Gellner JL (1992) Yield losses in winter-wheat caused by low-density cereal aphid populations. Agron J 84(2):180–183. https://doi.org/10.2134/agronj1992.00021962008400020011x
Kieckhefer R, Kantack B (1980) Losses in yield in spring wheat in South Dakota caused by cereal aphids. J Econ Entomol 73(4):582–585. https://doi.org/10.1093/jee/73.4.582
Kieckhefer RW, Dickmann DA, Miller EL (1976) Color responses of cereal aphids. Ann Entomol Soc Am 69(4):721–724. https://doi.org/10.1093/aesa/69.4.721
Kim W, Johnson JW, Baenziger PS, Lukaszewski AJ, Gaines CS (2004) Agronomic effect of wheat-rye translocation carrying rye chromatin (1R) from different sources. Crop Sci 44(4):1254–1258. https://doi.org/10.2135/cropsci2004.1254
Kogan M, Ortman EF (1978) Antixenosis—a new term proposed to define Painter’s “non-preference” modality of resistance. Bull Entomol Soc Am 24:175–176. https://doi.org/10.1093/besa/24.2.175
Lage J, Skovmand B, Andersen SB (2003) Characterization of greenbug (Homoptera: Aphididae) resistance in synthetic hexaploid wheats. J Econ Entomol 96(6):1922–1928. https://doi.org/10.1093/jee/96.6.1922
Lage J, Skovmand B, Andersen S (2004) Resistance categories of synthetic hexaploid wheats resistant to the Russian wheat aphid (Diuraphis noxia). Euphytica 136(3):291–296. https://doi.org/10.1023/B:EUPH.0000032732.53350.93
Leather SR, Dixon AFG (1984) Aphid growth and reproductive rates. Entomol Exp Appl 35(2):137–140. https://doi.org/10.1111/j.1570-7458.1984.tb03373.x
Liu X, Yang X, Wang C, Wang Y, Zhang H, Ji W (2011) Molecular mapping of resistance gene to English grain aphid (Sitobion avenae F.) in Triticum durum wheat line C273. Theor Appl Genet 124(2):287–293. https://doi.org/10.1007/s00122-011-1704-7
Lu H, Rudd JC, Burd JD, Weng Y (2010) Molecular mapping of greenbug resistance genes Gb2 and Gb6 in T1AL.1RS wheat-rye translocations. Plant Breed 129(5):472–476. https://doi.org/10.1111/j.1439-0523.2009.01722.x
Macaulay M, Ramsay L, Åhman I (2020) Quantitative trait locus for resistance to the aphid Rhopalosiphum padi L. in barley (Hordeum vulgare L.) is not linked with a genomic region for gramine concentration. Arthropod Plant Interact 14(1):57–65. https://doi.org/10.1007/s11829-019-09727-7
Marimuthu M, Smith CM (2012) Barley tolerance of Russian wheat aphid (Hemiptera: Aphididae) biotype 2 herbivory involves expression of defense response and developmental genes. Plant Signal Behav 7(3):382–391. https://doi.org/10.4161/psb.19139
Mater Y, Baenziger S, Gill K, Graybosch R, Whitcher L, Baker C, Specht J, Dweikat I (2004) Linkage mapping of powdery mildew and greenbug resistance genes on recombinant IRS from ‘Amigol’ and ‘Kavkaz’ wheat-rye translocations of chromosome 1RS.1AL. Genome 47(2):292–298. https://doi.org/10.1139/g03-101
McIntosh RA, Yamazaki Y, Dubcovsky J, Rogers WJ, Morris C, Appels R, Xia X (2013) Catalogue of gene symbols for wheat. In: Proceedings of 12th international wheat genetics symposium, Yokohama
Migui SM, Lamb RJ (2003) Patterns of resistance to three cereal aphids among wheats in the genus Triticum (Poaceae). Bull Entomol Res 93(4):323–333. https://doi.org/10.1079/BER2003246
Migui SM, Lamb RJ (2004) Seedling and adult plant resistance to Sitobion avenae (Hemiptera: Aphididae) in Triticum monococcum (Poaceae), an ancestor of wheat. Bull Entomol Res 94(1):35–46. https://doi.org/10.1079/BER2003278
Mitchell EAD, Mulhauser B, Mulot M, Mutabazi A, Glauser G, Aebi A (2017) A worldwide survey of neonicotinoids in honey. Science 358:109–111. https://doi.org/10.1126/science.aan3684
Moharramipour S, Tsumuki H, Sato K, Murata S, Kanehisa K (1997) Effects of leaf color, epicuticular wax and gramine content in barley hybrids on aphid populations. Appl Entomol Zool 32:1–8. https://doi.org/10.1303/aez.32.1
Ni X, Quisenberry SS (2000) Comparison of DIMBOA concentrations among wheat isolines and corresponding plant introduction lines. Entomol Exp Appl 96(3):275–279. https://doi.org/10.1046/j.1570-7458.2000.00706.x
Ni XZ, Quisenberry SS, Heng-Moss T, Markwell J, Higley L, Baxendale F, Sarath G, Klucas R (2002) Dynamic change in photosynthetic pigments and chlorophyll degradation elicited by cereal aphid feeding. Entomol Exp Appl 105(1):43–53. https://doi.org/10.1046/j.1570-7458.2002.01031.x
Painter RH (1941) The economic value and biologic significance of insect resistance in plants. J Econ Entomol 34(3):358–367. https://doi.org/10.1093/jee/34.3.358
Pereira RRC, Moraes JC, Prado E, Dacosta RR (2010) Resistance inducing agents on the biology and probing behaviour of the greenbug in wheat. Sci Agric 67(4):430–434. https://doi.org/10.1590/S0103-90162010000400009
Pettersson J, Pickett J, Pye B, Quiroz A, Smart L, Wadhams L, Woodcock C (1994) Winter host component reduces colonization by bird-cherry-oat aphid, Rhopalosiphum padi (L.) (Homoptera, Aphididae), and other aphids in cereal fields. J Chem Ecol 20(10):2565–2574. https://doi.org/10.1007/BF02036192
Pettersson J, Tjallingii WF, Hardie J (2007) Host-plant selection and feeding. In: VanEmden HF et al (eds) Aphids as crop pests. Cabi Publishing, Wallingford, pp 87–113
Pickett JA, Glinwood RT (2007) Chemical ecology. In: VanEmden HFHR (ed) Aphids as crop pests. Cabi Publishing, Wallingford, pp 235–260
Porter DR, Burd JD, Shufran KA, Webster JA, Teetes GL (1997) Greenbug (Homoptera: Aphididae) biotypes: selected by resistant cultivars or preadapted opportunists? J Econ Entomol 90(5):1055–1065. https://doi.org/10.1093/jee/90.5.1055
Porter DR, Burd JD, Shufran KA, Webster JA (2000) Efficacy of pyramiding greenbug (Homoptera: Aphididae) resistance genes in wheat. J Econ Entomol 93(4):1315–1318. https://doi.org/10.1603/0022-0493-93.4.1315
Porter DR, Harris MO, Hesler LS, Puterka GJ (2009) Insects which challenge global wheat production. In: Carver BF (ed) Wheat science and trade. Wiley-Blackwell, Iowa, pp 189–201
Powell G, Hardie J (2001) The chemical ecology of aphid host alternation: how do return migrants find the primary host plant? Appl Entomol Zool 36(3):259–267. https://doi.org/10.1303/aez.2001.259
Powell G, Tosh CR, Hardie J (2006) Host plant selection by aphids: behavioral, evolutionary, and applied perspectives. Ann Rev Entomol 51:309–330. https://doi.org/10.1146/annurev.ento.51.110104.151107
Rabbing R, Drees EM, Van der Graaf M, Verberne FCM, Wesselo A (1981) Damage effects of cereal aphids in wheat. Neth J Plant Pathol 87:217–232
Randolph TL, Peairs F, Weiland A, Rudolph JB, Puterka GJ (2009) Plant responses to seven Russian wheat aphid biotypes (Hemiptera: Aphididae) biotypes found in the United States. J Econ Entomol 102:1954–1959. https://doi.org/10.1603/029.102.0528
Riedell WE, Kieckhefer RW, Langham MA, Hesler LS (2003) Root and shoot responses to bird cherry-oat aphids and barley yellow dwarf virus in spring wheat. Crop Sci 43(4):1380–1386. https://doi.org/10.2135/cropsci2003.1380
Rosenthal J, Kotanen P (1994) Terrestrial plant tolerance to herbivory. Trends Ecol Evol 9(4):145–148. https://doi.org/10.1016/0169-5347(94)90180-5
Singh B, Deol GS (2003) Quantative grain yield losses caused by aphid complex in wheat. Crop Res 26(3):501–504
Singh B, Kaur J (2017) Compatibility of different pesticides used for aphid and stripe rust control in wheat. J Wheat Res 9(1):54–59
Singh B, Singh S (2009) Screening and identification of source of resistance against corn leaf aphid (Rhopalosiphum maidis Fitch.) in barley. Indian J Entomol 71(3):255–258
Singh RP, Trethowan R (2007) Breeding spring bread wheat for irrigated and rainfed production systems of the developing world. In: Kang MS et al (eds) Breeding major food staples. BlackWell Publishing, Iowa, pp 107–140. https://doi.org/10.1002/9780470376447
Singh B, Dhindsa GS, Singh H (2006) Screening of barley (Hordeum vulgare) germplasm against corn leaf aphid, Rhopalosiphum maidis (Fitch.). J Crop Improv 33(1):58–61
Singh B, Kaur S, Chunneja P (2018) Evaluation of plant resistance in progenitors of wheat against foliage feeding aphids (Rhopalosiphum padi L. and R. maidis Fitch.) in Punjab. Agric Res J 55(1):117–121. https://doi.org/10.5958/2395-146X.2018.00019.4
Singh B, Simon A, Kirstie H, Kurup S, Clark S, Aradottir G (2020) Characterization of bird cherry-oat aphid (Rhopalosiphum padi L.) behaviour and aphid host preference in relation to partially resistant and susceptible wheat landraces. Ann Appl Biol 177(2):184–194. https://doi.org/10.1111/aab.12616
Smith CM (2005) Plant resistance to arthropods: molecular and conventional approaches. Springer, Dordrecht
Smith CM, Starkey S (2003) Resistance to greenbug (Heteroptera: Aphididae) biotype I in Aegilops tauschii synthetic wheats. J Econ Entomol 96(5):1571–1576. https://doi.org/10.1093/jee/96.5.1571
Smith CM, Havlickova H, Starkey S, Gill BS, Holubec V (2004) Identification of Aegilops germplasm with multiple aphid resistance. Euphytica 135(3):265–273. https://doi.org/10.1023/B:EUPH.0000013306.15133.33
Snelling RO (1941) Resistance of plants to insect attack. Bot Rev 7(10):543–586
Sotelo P, Starkey S, Voothuluru P, Wilde GE, Smith CM (2009) Resistance to Russian wheat aphid biotype 2 in CIMMYT synthetic hexaploid wheat lines. J Econ Entomol 102(3):1255–1261. https://doi.org/10.1603/029.102.0352
Stenberg JA, Muola A (2017) How should plant resistance to herbivores be measured? Front Plant Sci 8:663. https://doi.org/10.3389/fpls.2017.00663
Stout MJ (2013) Re-evaluating the conceptual framework for applied research on host-plant resistance. Insect Sci 20:263–272. https://doi.org/10.1111/1744-7917.12011
Telang A, Sandström J, Dyreson E, Moran NA (1999) Feeding damage by Diuraphis noxia results in a nutritionally enhanced phloem diet. Entomol Exp Appl 91(3):403–412. https://doi.org/10.1046/j.1570-7458.1999.00508.x
Tremblay C, Cloutier C, Comeau A (1989) Resistance to the bird cherry-oat aphid, Rhopalosiphum padi L.(Homoptera: Aphididae), in perennial Gramineae and wheat x perennial Gramineae hybrids. Environ Entomol 18(6):921–923. https://doi.org/10.1093/ee/18.6.921
Voss TS, Kieckhefer RW, Fuller BW, McLeod MJ, Beck DA (1997) Yield losses in maturing spring wheat caused by cereal aphids (Homoptera: Aphididae) under laboratory conditions. J Econ Entomol 90(5):1346–1350. https://doi.org/10.1093/jee/90.5.1346
Watt A (1979) The effect of cereal growth stages on the reproductive activity of Sitobion avenae and Metopolophium dirhodum. Ann Appl Biol 91(2):147–157. https://doi.org/10.1111/j.1744-7348.1979.tb06485.x
Webster J, Inayatullah C, Hamissou M, Mirkes K (1994) Leaf pubescence effects in wheat on yellow sugarcane aphids and greenbugs (Homoptera: Aphididae). J Econ Entomol 87(1):231–240. https://doi.org/10.1093/jee/87.1.231
Weiland AA, Peairs FB, Ranpolph TL, Rudolph JB, Haley SD, Puterka GJ (2008) Biotypic diversity in Colorado Russian wheat aphid (Hemiptera: Aphididae) populations. J Econ Entomol 101(2):569–574. https://doi.org/10.1093/jee/101.2.569
Weng Y, Perumal A, Burd JD, Rudd JC (2010) Biotypic diversity in greenbug (Hemiptera: Aphididae): microsatellite-based regional divergence and host-adapted differentiation. J Econ Entomol 103(4):1454–1463. https://doi.org/10.1603/EC09291
Xu X, Li G, Carver BF, Armstrong JS (2020) Gb8, a new gene conferring resistance to economically important greenbug biotypes in wheat. Theor Appl Genet 133:615–622. https://doi.org/10.1007/s00122-019-03491-1
Yazdani M, Baker G, DeGraaf H et al (2017) First detection of Russian wheat aphid Diuraphis noxia Kurdjumov (Hemiptera: Aphididae) in Australia: a major threat to cereal production. Austral Entomol 57:410. https://doi.org/10.1111/aen.12292
Zhu LC, Smith CM, Fritz A, Boyko EV, Flinn MB (2004) Genetic analysis and molecular mapping of a wheat gene conferring tolerance to the greenbug (Schizaphis graminum Rondani). Theor Appl Genet 109(2):289–293. https://doi.org/10.1007/s00122-004-1632-x
Zhu LC, Smith CM, Fritz A et al (2005) Inheritance and molecular mapping of new greenbug resistance genes in wheat germplasms derived from Aegilops tauschii. Theor Appl Genet 111:831–837. https://doi.org/10.1007/s00122-005-0003-6
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2022 The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd.
About this chapter
Cite this chapter
Singh, B., Jasrotia, P., Crespo-Herreraa, L. (2022). Breeding for Aphid Resistance in Wheat: Status and Future Prospects. In: Kashyap, P.L., et al. New Horizons in Wheat and Barley Research . Springer, Singapore. https://doi.org/10.1007/978-981-16-4449-8_16
Download citation
DOI: https://doi.org/10.1007/978-981-16-4449-8_16
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-16-4448-1
Online ISBN: 978-981-16-4449-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)