Reviews and Progresses

Impact of Aphids on Cereals and Phloem Based Defense Mechanism  

Siddra  Ijaz1,2
1 Centre of Agricultural Biochemistry and Biotechnology (CABB), University of Agriculture Faisalabad, Pakistan
2 Department of Plant Sciences, University of California Davis, CA, USA
Author    Correspondence author
Molecular Plant Breeding, 2016, Vol. 7, No. 7   doi: 10.5376/mpb.2016.07.0007
Received: 14 Dec., 2015    Accepted: 18 Dec., 2015    Published: 05 Jan., 2016
© 2016 BioPublisher Publishing Platform
This is an open access article published under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Preferred citation for this article:

Siddra Ijaz, 2016, Impact of Aphids on Cereals and Phloem Based Defense Mechanism, Molecular Plant Breeding, 7(07): 1-5 (doi: 10.5376/mpb.2016.07.0007)

Abstract

A biological interaction is existed between host plant and phloem feeder. In this interaction, plant based defense responses are activated. These plant defense responses function in a variety of ways for hindering the invaders. In insect-plant interaction, recent researches focus on the interaction of aphids with their host plants and make them a model phloem feeder. Hence this review article is based on the consequences of aphid’s interaction to their host plants as well as phloem based defense mechanism that is activated in response of this interaction. 

Keywords
Aphids; Cereal; Barley; wheat; Phloem based defense mechanism

Introduction
Aphids are the most hostile insects to agricultural crops around the globe and cause economic loss of approximately $5 billion per annum (Matis et al., 2007). They are common pest of cereal crops; wheat, barley and oat. However, Rice is the secondary host of aphids. Rice crop is infested by aphid in the non-availability of primary hosts around. Aphids belong to order hemiptera and sucking phloem sap is the common characteristics of all insects belong to this order. Aphids suck phloem sap as their food source, hence named as phloem feeding insects. Plant tissue integrity is breached when phytophages such as aphids take nutrients and photoassimilates from phloem sap of foliages (Walling, 2000). They provide challenges to plants by depleting photosynthates, and introducing various chemical compounds such as protein effectors that modify plant defense signaling (Kaloshian and Walling, 2005). These phloem feeders have special mechanism of feeding. Aphids also take benefit of their skilled and proficient feeding strategies for deterring many plant defenses. For combating with plant defense systems, aphids adopt different illusory strategies (daCunha et al., 2007) by delivering proteins/chemical compounds into plant that effect wound healing and other defense-signaling networks. Due to the introduction of effectors into plants by aphids, various cellular and biochemical processes are influenced that enhance the success rate of aphids on their host plant. In plant-insect interaction, there are three stages of interactions viz., pre-entry, entry, and colonization that are influenced by effectors. These stages are important for adaptations and deceptive plans employed by phloem-feeders. In this interaction, salivary secretion of insect has been suggested as a key factor (Walling, 2008).
 
1 Impact of Aphid on Wheat
Wheat (Triticum aestivum) is a most important cereal crop and staple food world wide (Khan et al., 2000). There is an incessant need of achieving higher yield for feeding increasing population of the world because being a staple food; it is required for more than 35% of the world population (Khakwani et al., 2012). Various biotic and abiotic factors are responsible for its low yield and among insect pests, 29 aphid species infest this crop (Geza, 2000). Upon aphid attack, emerging heads as well as awns are trapped by this insect and flag leaf is rolled that result in poor pollination. Aphid attack begins from emergence and persists till maturity (Shea et al., 2000).
 
Aphid is becoming a serious threat to wheat crop and according to literature this insect has started wheat crop feeding even at milky grain stage when no insecticidal spray is recommended. Aphids attack on aerial parts from one shoot stage to grain ripening stage and result in necrosis and chlorosis by repressing photosynthesis process in aerial parts of wheat crop. Aphid cause chlorosis, curling and distortion of leaves and shoot by sucking sap present in these parts and result in stunted growth of this crop and lessen grain yield (Hong and Ding, 2007). Aphids hit wheat crop both directly and indirectly by sucking sap from it and by transmitting fungal disease into it. So there is dire need to establish proactive strategies for protecting wheat crop from this caustic insect.
 
2 Impact of Aphid on Barley
Barley is grown on diverse geographical areas and in terms of area and production, it ranks at 4th after other cereals such as wheat, rice and maize. It is tolerant crop that resists harsh conditions well as compared to other crops and also yields more output by applying less input. However, barley is also affected and targeted by aphids that limit growth and yield of this crop. Aphids, as viral vectors also affect barley crop by transmitting viruses. Barley like other crop plants possesses an arsenal of chemical and physical defenses for the sake of self protection (Diaz et al., 2014). In aphid affected barley crops, various barriers such as waxes, acontic phenolics, gramine etc have been observed (Larsson et al., 2011).
 
3 Aphid’s Approaches against Phloem Located Defense
Aphids select host plant by using visual and olfactory signals for their shelter, feeding and even for oviposition (Powell et al., 2006). Aphids have multibranched stylet sheath that depict the stylet route to phloem is not straight and is tortuous (Tjallingii, 2006). Upon plant selection, they face exposure to various chemicals of cuticular wax. These chemicals are secondary metabolites and volatile as well as non-volatile compounds that may attract or even repel the insects (Müller and Riederer, 2005). Leaf trichomes also take part in this intricate situation by discharging secondary metabolites and other compounds having antibiotic or antixenotic properties (Wagner et al., 2004).
 
Aphids secrete saliva to dissolve chemicals compound on leaf surface for determining the physical characteristics and chemical defense of host plant (Miles, 1999). These probing behaviors adopted by insects help them to sense the difference in cell wall contents such as carbohydrate, secondary metabolites and epicuticular waxes for determining non-host or/ host status (Müller and Riederer, 2005). However stylet progression path determines constitutive and induced defenses an insect encounters while defense signaling mechanism induced in attacked plant and protein or/metabolites that are accumulated in this infested host are determined by the nature and properties of salivary compounds or/effectors (Freeman et al., 2001). Two saliva types, gel like and watery are possessed by aphids though their chemical composition is being somewhat overlapped (Miles, 1999; Will et al., 2012). They use salivary secretions as gustatory cues or signals for assessing and evaluating the apoplast’s chemical compositions that provide advanced informations and directionality to insects regarding host aptness for feeding as well as oviposition and stylet movement respectively (Lei et al., 1998). When aphid pierces a phloem sieve element through stylet then the plasma membrane lesion must be plugged and repaired swiftly by depositing callose and plugging proteins to thwart the phloem sap leakage into apoplast (Will and van Bel, 2006) but aphids alter these responses to augment their own success. Thus the shutting of stylet-induced lesions can spontaneously obstruct an insect’s food canal. Hence, it is not astonishing that aphids antagonize the cytosolic wound-healing process (Will et al., 2007).
 
4 Phloem Based Defense Mechanism
In phloem feeding a unique biological interaction is engrossed between phloem feeder and its host plant. During this interaction plant based defense responses are induced and among these, activation of salicylic acid signaling pathway is most promising however its molecular bases are not yet cleared. Phloem-feeding insects such as aphids that is an archetypal group of phloem feeders, exhibit highly specialized mode of feeding and generate a unique stress on plant vigor (Tjallingii, 2006; Will and van Bel, 2008; De Vos and Jander, 2009). The stress due to phloem feeders like aphids is crushing to the production and yield of agriculturally important crops, such as wheat (Will and van Bel, 2006). Phloem feeding insects such as aphids, infiltrate their stylet-like mouthparts into epidermal and mesophyll cell layers for feeding photoassimilates that are being translocated in the phloem sieve elements (Pollard, 1972; Dixon, 1998). Aphids on sucking phloem sap can transmit viruses to host plant and even inject toxins into it.
 
Using phloem-based defense mechanism, plants secure themselves to devastating threat pose by phloem-feeding insects on attack. Phloem feeders on feeding induce a specialized mechanism and defensive response in plants such as toxic metabolites production, defensive proteins production at high rate and modulating the nutritional status of plants. The phloem based defense response is involved the coordinated expression of two genes, PP2-A and GSL5 that encode phloem lectin protein PP2-A and β-1,3- glucan synthase GSL5 respectively ( et al., 2011; Zhang et al., 2011). Phloem protein 2 (PP2) is amongst the most bountiful proteins in phloem sap. Upon the dimerization of pp2-A protein, it is associated with another phloem protein, PP1 and a high molecular weight polymer is formed and accumulated for blocking phloem sieve plate pores (Kehr, 2006; Will et al., 2007; Beneteau et al., 2010) accompanying with this process, β-1, 3-glucan callose is synthesized by GSL5 that further coagulated on sieve plates for closure their pores thus hamper aphid phloem feeding ( et al., 2013). Hence, PP2-A and GSL5 are requisite and crucial components of the phloem-based defense mechanism. According to literature, phloem-based defense mechanism is weakened in plants treated by ethylene signaling inhibitors that reveal ethylene signaling pathway is required for this response.
 
Though, impediment of aphid phloem sap feeding is achieved on closing the sieve plates pores by AtPP2–PP1 polymer complexes and GLS5-mediated callose coagulation but it is generally induced by harpin protein. In harpin response, recruitment of ethylene signaling regulator, EIN2 and the transcription factor MYB44 (co-regulator) by ethylene signaling pathways confer phloem-based defense against aphid (Zhang et al., 2011; et al., 2013). Transcription of EIN2 gene is activated by the binding of MYB44 transcription factor (Qiao et al., 2012). Harpins have multiple effects in plants and inducing resistance against insects, particularly aphid, is one of these (Zhang et al., 2011). Harpins induced defense response against aphid is synchronized by ethylene signaling pathway ( et al., 2013). However crosstalk among different hormonal signaling pathways is also being characterized to its multiple effects (Chen et al., 2008). Various research reports suggested that 10-42 residue fragment of N-terminal region of hpaI (harpin protein) is more effective for inducing defense response or resistance (Wang et al., 2008).
 
5 Sieve Tube Occlusion Mechanisms in Plants
Sieve tube occlusion mechanism is involved in the impediment of phytopahtogens by sieve pores plugging to thwart their entry and invading from injured regions thereby preventing the loss of sap in sieve tubes (van Bel, 2003).  In plants, two kinds of sieve tube occlusion mechanisms are existed; protein plugging and callose deposition (Will and van Bel, 2006; Furch et al., 2007). Callose is a linear β-1, 3-glucan polymer and is formed in an enzymatic reaction mediated via callose synthase in the presence of Ca2+. Callose is deposited extracellularly around the sieve pores as collars (Zabotin et al., 2002). Besides the callose deposition, sieve pores occlusion is also achieved via specialized group of proteins (Will and van Bel, 2006). These are basically phloem proteins (PP) that facilitate and allow the swift occlusion of sieve tubes (Ernst et al., 2012). Upon oxidation these phloem proteins (PP1 and PP2) produce aggregates of insoluble nature via cross-linking, making polymers of high molecular-weight that occlude sieve pores of wounded sieve tubes (Read and Northcote, 1983; Alosi et al., 1988). Owing to interaction of phloem proteins (PPs) in the presence of Ca2+ and oxygen, sieve tubes and injured sites are rapidly occluded by gelling of the exudates (Furch et al., 2010).
 
6 Outlooks
Phloem feeding insects like aphids pose serious fatalities to agriculture due to their broad host range, highly specialized feeding strategies and rapidly evolving insecticide-resistant strains. Due to these attributes, aphids overwhelm plant defense system. The emerging genomics resources and advanced approaches in molecular biology will divulge the factors relating innate immunity and signaling network involved as well as gene-for-gene interaction that evoke plant defense to phloem feeders. Current researches and deep understanding about the plant defense responses stimulated and activated by phloem feeders will bestow clear, improved and new insights into the complexity and dynamics of plant insect interactions.
 
References
Alosi M.C., Melroy D.L., and Park R.B., 1988, The regulation of gelation of phloem exudates from Cucurbita fruit by dilution, glutathione, and glutathione reductase, Plant Physiol. 86(4), 1089–1094
http://dx.doi.org/10.1104/pp.86.4.1089
 
Beneteau J., Renard D., Marche L., Douville E., Lavenant L., Rahbe Y., Dupont D., Vilaine F., and Dianat S., 2010, Binding properties of the N-acetylglucosamine and high-mannose N-glycan PP2-A1 phloem lectin in Arabidopsis, Plant Physiol, 153(3): 1345–1361
http://dx.doi.org/10.1104/pp.110.153882
 
Chen L., Qian J., Qu S.P., Long J.Y., Yin Q., Zhang C.L., Wu X.J., Sun F., Wu T.Q., Hayes M., Beer S.V., and Dong H.S., 2008, Identification of specific fragments of HpaGXooc, a harpin from Xanthomonas oryzae pv. oryzicola, that induce disease resistance and enhance growth in plants, Phytopathology 98(7): 781–791
http://dx.doi.org/10.1094/PHYTO-98-7-0781
 
Cunha D.L., Sreerekha M.V., and Mackey D., 2007, Defense suppression by virulence effectors of bacterial phytopathogens, Curr. Opin. Plant. Biol. 10(4):349–357
http://dx.doi.org/10.1016/j.pbi.2007.04.018
 
Daiz I., Cambra I., Santamria M.E., Gonzalez-Melendi P., and Martinez M., 2014, Responses to Phytophagous Arthropods. J. umlehn, N. Slein (eds). Biotechnological Approaches to Barley Improvement. Biotechnology in Agriculture and Forestry 69. DOI. 10. 1007/978-3-662-44406-1_12.
Martin D.V., and Georg J., 2009, Myzus persicae (green peach aphid) salivary components induce defence responses in Arabidopsis thaliana, Plant Cell Environ. 32(11): 1548–1560
http://dx.doi.org/10.1111/j.1365-3040.2009.02019.x
 
Dixon A.F.G., 1998, Aphid Ecology: An Optimization Approach, Ed 2. Chapman and Hall, New York
Ernst A.M., Jekat S.B., Zielonka S., Müller B., Neumann U., Rüping B., Twyman R.M., Krzyzanek V., Prüfer D., and Noll G.A., 2012, Sieve element occlusion (SEO) genes encode structural phloem proteins involved in wound sealing of the phloem, Proc. Natl. Acad. Sci. U.S.A., 109(28): 1980–1989
http://dx.doi.org/10.1073/pnas.1202999109
 
Freeman T.P., Buckner J.S., Nelson D.R., Chu C-c. & Henneberry T.J., 2001, Stylet penetration by Bemisia argentifolii (Homoptera: Aleyrodidae) into host leaf tissue, Annals of the Entomological Society of America, 94(5): 761–768
http://dx.doi.org/10.1603/0013-8746(2001)094[0761:SPBBAH]2.0.CO;2
 
Furch A.C.U., Hafke J.B., Schulz A. and van Bel A.J.E., 2007, Ca2+- mediated remote control of reversible sieve tube occlusion in Vicia faba, J. Exp. Bot., 58(11): 2827–2838
http://dx.doi.org/10.1093/jxb/erm143
 
Furch A.C.U., Zimmermann M.R., Will T., Hafke J.B. and van Bel A.J.E., 2010, Remote-controlled stop of phloem mass flow by biphasic occlusion in Cucurbita maxima, J. Exp. Bot. 61(13): 3697–3708
http://dx.doi.org/10.1093/jxb/erq181
 
Geza K., 2000, Aphid flight and change in abundance of winter wheat pests, Archives phytopatholgy, Plant Prot., 33(33): 361-373
 
Hong X.Y., and Ding J.H., 2007, Agricultural entomology, 2nd edn. (In Chinese), Beijing: China Agricultural Press, 114–119
 
Kaloshian I., and Walling L.L., 2005, Hemipterans as plant pathogens, Annu Rev Plant Biol. 43(43): 491–521
http://dx.doi.org/10.1146/annurev.phyto.43.040204.135944
 
Kehr J., 2006, Phloem sap proteins: their identities and potential roles in the interaction between plants and phloem-feeding insects, J. Exp. Bot, 57(4): 767–774
http://dx.doi.org/10.1093/jxb/erj087
 
Khakwani A.A., Dennett M.D., Munir M., and Abid M., 2012, Growth and yield response of wheat varieties to water stress at booting and anthesis stages of development, Pak. J. Bot., 44(3): 879-886
 
Khan M.A., Hussain I., and Baloch M.S., 2000, Wheat yield potential-current status and future strategies, Pak. J. Biol. Sci., 3(1): 82-86
http://dx.doi.org/10.3923/pjbs.2000.82.86
 
Laarsson K.A.E., Saheed S.A., Gradin T., Delp G., Karpinska B., Botha C.E. J., and Jonsson L.M.V., 2011, Diffrential regulation of 3-aminomethyl/N-methyl-3-aminomethylindole N-methyltransferase and gramine in barley by both biotic and biotic stress conditions, Plant Physiology and Biochemistry, 49(1): 96-102
http://dx.doi.org/10.1016/j.plaphy.2010.10.005
 
Lei H., Xu R., Tjallingii W.F., and Van Lenteren J.C., 1998, Electrical penetration graphs of greenhouse whitefly, Trialeurodes vaporariorum (Westwood), Acta Entomol Sin, 41: 113–123
 
Lü B., Li X., Sun W.W., Li L., Gao R., Zhu Q., Tian S.M., Fu M.Q., Yu H.L., Tang X.M., Zhang C.L., and Dong H.S., 2013, AtMYB44 regulates resistance to the green peach aphid and diamondback moth by activating EIN2-affected defenses in Arabidopsis, Plant Biology (Stuttgart), 15(5): 841–850
http://dx.doi.org/10.1111/j.1438-8677.2012.00675.x
 
Lü B., Sun W., Zhang S., Zhang C., Qian J., Wang X., Gao R. and Dong H., 2011, HrpNEa-induced deterrent effect on phloem feeding of the green peach aphid Myzus persicae requires AtGSL5 and AtMYB44 genes in Arabidopsis thaliana, Journal of Biosciences, 36(1): 127–137.
http://dx.doi.org/10.1007/s12038-011-9016-2
 
Matis J.H., Kiffe T.R., Matis T.I., and Stevenson D.E., 2007, Stochastic modeling of aphid population growth with non linear, power-law dynamics, Mathematical Biosciences, 208(2): 469-494
http://dx.doi.org/10.1016/j.mbs.2006.11.004
 
Miles P.W., 1999, Aphid saliva, Biol. Rev. Camb. Philos. Soc., 74(1): 41–85
http://dx.doi.org/10.1017/S0006323198005271
 
Mülle C., and Riederer M., 2005, Plant surface properties in chemical ecology, J Chem Ecol, 31(11): 2621–2651
http://dx.doi.org/10.1007/s10886-005-7617-7
 
Pollard D.G., 1972, Plant penetration by feeding aphids (Hemiptera, Aphidoidea): A review, Bull. Entomol. Res., 62(04): 631–714
http://dx.doi.org/10.1017/S0007485300005526
 
Powell G., Tosh C.R., and Hardie J., 2006, Host plant selection by aphids: behavioral, evolutionary, and applied perspectives, Annu Rev Entomol 51(1): 309–330
http://dx.doi.org/10.1146/annurev.ento.51.110104.151107
 
Qiao H., Shen Z.X., Huang S.S., Schmitz R.J., Urich M.A., Briggs S.P., and Ecker J.R., 2012, Processing and subcellular trafficking of ER-tethered EIN2 control response to ethylene gas, Science. 338(6105): 390–393
http://dx.doi.org/10.1126/science.1225974
 
Read S.M., and Northcote D.H., 1983, Subunit structure and interactions of the phloem proteins of Cucurbita maxima (pumpkin), Eur J Biochem, 134(3): 561-569
http://dx.doi.org/10.1111/j.1432-1033.1983.tb07603.x
 
Shea G., Botha J., and Hardie D., 2000, Russian wheat aphid: An exotic threat to Western Australia, Fact Sheet, www.agric.wa.gov.au.
 
Tjallingii W.F., 2006, Salivary secretions by aphids interacting with proteins of phloem wound responses, J. Exp. Bot, 57(4):739–745
http://dx.doi.org/10.1093/jxb/erj088
 
Van Bel A.J.E., 2003, The phloem, a miracle of ingenuity, Plant. Cell. Environ., 26(1): 125–149
http://dx.doi.org/10.1046/j.1365-3040.2003.00963.x
 
Wagner G.J., Wang E., and Shepherd R.W., 2004, New approaches for studying and exploiting an old protuberance, the plant trichome, Ann Bot (Lond), 93(1): 3–11
http://dx.doi.org/10.1093/aob/mch011 
 
Walling L.L., 2000, The myriad plant responses to herbivores, J Plant Growth Regul., 19(2):195–216
 
Walling L.L., 2008, Avoiding effective defenses: strategies employed by phloem-feeding insects, Plant Physiol. 146(3): 859–866
http://dx.doi.org/10.1104/pp.107.113142
 
Wang Y., Tang M., Hao P.Y., Yang Z.F., Zhu L.L., and He G.C., 2008, Penetration into rice tissues by brown plant hopper and fine structure of the salivary sheaths, Entomol. Exp. Appl., 129(3): 295–307
http://dx.doi.org/10.1111/j.1570-7458.2008.00785.x
 
Will T., and van Bel A.J.E., 2006, Physical and chemical interactions between aphids and plants, J. Exp. Bot., 57: 729–737
http://dx.doi.org/10.1093/jxb/erj089
 
Will T., and van Bel A.J.E., 2008, Induction as well as suppression: how aphid saliva may exert opposite effects on plant defense, Plant. Signal. Behav., 3(6): 427–430
http://dx.doi.org/10.4161/psb.3.6.5473
 
Will T., Tjallingii W.F., Thonnessen A., and van Bel A.J.E., 2007, Molecular sabotage of plant defense by aphid saliva, Proc Natl Acad Sci USA, 104(25): 10536–10541
http://dx.doi.org/10.1073/pnas.0703535104
 
Will T., Steckbauer K., Hardt M., and van Bel A.J.E., 2012, Aphid gel saliva: sheath structure, protein composition, and secretors dependence on stylet-tip milieu. PLoS ONE, 7(10):e46903
http://dx.doi.org/10.1371/journal.pone.0046903
 
Will T., Tjallingii W.F., Thönnessen A., and van Bel A.J.E., 2007, Molecular sabotage of plant defense by aphid saliva, Proc. Natl. Acad. Sci.U.S.A., 104(25): 10536–10541
http://dx.doi.org/10.1073/pnas.0703535104
 
Zabotin A.I., Barysheva T.S., Trofimova O.I., Lozovaya V.V., and Widholm J., 2002, Regulation of callose metabolism in higher plant cells in vitro, Russ. J. Plant Physiol., 49(6): 792–798
http://dx.doi.org/10.1023/A:1020969730151
 
Zhang C., Shi H., Chen L., Wang X., Lü B., Zhang S., Liang Y., Liu R., Qian J., Sun W., You Z., and Dong H., 2011, Harpin-induced expression and transgenic over expression of the phloem protein gene AtPP2-A1 in Arabidopsis repress phloem feeding of the green peach aphid Myzus persicae, BMC Plant. Biol., 11:11
http://dx.doi.org/10.1186/1471-2229-11-11

 

Molecular Plant Breeding
• Volume 7
View Options
. PDF(247KB)
. FPDF
. HTML
. Online fPDF
Associated material
. Readers' comments
Other articles by authors
pornliz suckporn porndick pornstereo . Siddra  Ijaz
Related articles
. Aphids
. Cereal
. Barley
. wheat
. Phloem based defense mechanism
Tools
. Email to a friend
. Post a comment