A color morph-specific salivary carotenoid desaturase enhances plant photosynthesis and facilitates phloem feeding of Myzus persicae (Sulzer).

Publisher: Published for SCI by Wiley Country of Publication: England NLM ID: 100898744 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1526-4998 (Electronic) Linking ISSN: 1526498X NLM ISO Abbreviation: Pest Manag Sci Subsets: MEDLINE

Original Publication: West Sussex, UK : Published for SCI by Wiley, c2000-

Aphids*/physiology ; Aphids*/genetics ; Phloem*/metabolism ; Photosynthesis*; Animals ; Nicotiana/genetics ; Pigmentation/genetics ; Oxidoreductases/metabolism ; Oxidoreductases/genetics ; Insect Proteins/metabolism ; Insect Proteins/genetics ; Feeding Behavior ; Carotenoids/metabolism ; Saliva/metabolism ; Color

Background: Body-color polymorphisms in insects are often explained by environmental selective advantages. Differential fitness related to body coloration has been demonstrated in Myzus persicae (Sulzer): performance of the red morph is in general better than that of the green morph on tobacco plants. However, the molecular mechanism involved is largely unclear.
Results: Here we showed that the red morph of M. persicae had higher expression of a carotenoid desaturase CarD763 in the whole body, salivary gland and saliva relative to the green morph. Also, 18% individuals displayed faded red body color 5 days post dsCarD763 treatment. Furthermore, knockdown of CarD763 in the red morph significantly prolonged the time needed to locate phloem and shortened the duration of phloem feeding. Honeydew production and survival rate decreased as well. In contrast, overexpression of CarD763 in tobacco leaves facilitated aphid feeding, enhanced honeydew production and improved the survival rate of aphids. Compared with those fed by dsGFP aphids, plants infested by dsCarD763-treated aphids had higher ROS accumulation, lower lycopene content and photosynthetic rate, and maximum photon quantum yield. The reverse was true when plants overexpressed CarD763.
Conclusion: These findings demonstrated that CarD763, a red morph-specific salivary protein, could enhance aphid feeding and early colonization by promoting plant photosynthesis. © 2024 Society of Chemical Industry.
(© 2024 Society of Chemical Industry.)

Henter HJ and Via S, The potential for coevolution in a host‐parasitoid system. i. genetic variation within an aphid population in susceptibility to a parasitic wasp. Evolution 49:427–438 (1995).
Araya JE, Cambron SE and Ratcliffe RH, Development and reproduction of two color forms of English grain aphid (Homoptera: Aphididae). Environ Entomol 25:366–369 (1996).
Losey JE, Ives AR, Harmon J, Ballantyne F and Brown C, A polymorphism maintained by opposite patterns of parasitism and predation. Nature 388:269–272 (1997).
Bass C, Zimmer CT, Riveron JM, Wilding CS, Wondji CS, Kaussmann M et al., Gene amplification and microsatellite polymorphism underlie a recent insect host shift. Proc Natl Acad Sci U S A 110:19460–19465 (2013).
Ramsey JS, Elzinga DA, Sarkar P, Xin YR, Ghanim M and Jander G, Adaptation to nicotine feeding in Myzus persicae. J Chem Ecol 40:869–877 (2014).
Singh KS, Troczka BJ, Duarte A, Balabanidou V, Trissi N, Carabajal Paladino LZ et al., The genetic architecture of a host shift: an adaptive walk protected an aphid and its endosymbiont from plant chemical defenses. Sci Adv 6:e1070 (2020).
Jenkins RL, Loxdale HD, Brookes CP and Dixon AFG, The major carotenoid pigments of the grain aphid, Sitobion avenae (F.) (Hemiptera: Aphididae). Physiol Entomol 24:171–178 (1999).
Tsuchida T, Molecular basis and ecological relevance of aphid body colors. Curr Opin Insect Sci 17:74–80 (2016).
Cobbs C, Heath J, Stireman JO and Abbot P, Carotenoids in unexpected places: gall midges, lateral gene transfer, and carotenoid biosynthesis in animals. Mol Phylogenet Evol 68:221–228 (2013).
Moran NA and Jarvik T, Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science 328:624–627 (2010).
Bryon A, Kurlovs AH, Dermauw W, Greenhalgh R, Riga M, Grbic M et al., Disruption of a horizontally transferred phytoene desaturase abolishes carotenoid accumulation and diapause in Tetranychus urticae. Proc Natl Acad Sci USA 114:5871–5880 (2017).
Guo H, Zhang Y, Tong J, Ge P, Wang Q, Zhao Z et al., An aphid‐secreted salivary protease activates plant defense in phloem. Curr Biol 30:4826–4836 (2020).
Bos JI, Prince D, Pitino M, Maffei ME, Win J and Hogenhout SA, A functional genomics approach identifies candidate effectors from the aphid species Myzus persicae (green peach aphid). PLoS Genet 6:e1001216 (2010).
Chaudhary R, Atamian HS, Shen Z, Briggs SP and Kaloshian I, GroEL from the endosymbiont Buchnera aphidicola betrays the aphid by triggering plant defense. Proc Natl Acad Sci USA 111:8919–8924 (2014).
Rodriguez PA, Escudero‐Martinez C and Bos JI, An aphid effector targets trafficking protein VPS52 in a host‐specific manner to promote virulence. Plant Physiol 173:1892–1903 (2017).
Li Q, Fu Y, Liu X, Sun J, Hou M, Zhang Y et al., Activation of wheat defense response by Buchnera aphidicola‐derived small chaperone protein GroES in wheat aphid saliva. J Agric Food Chem 70:1058–1067 (2022).
Guo H, Zhang Y, Li B, Li C, Shi Q, Zhu‐Salzman K et al., Salivary carbonic anhydrase II in winged aphid morph facilitates plant infection by viruses. Proc Natl Acad Sci USA 120:e2222040120 (2023).
Louis J, Leung Q, Pegadaraju V, Reese J and Shah J, PAD4‐dependent antibiosis contributes to the ssi2‐conferred hyper‐resistance to the green peach aphid. Mol Plant Microbe Interact 23:618–627 (2010).
Louis J, Gobbato E, Mondal HA, Feys BJ, Parker JE and Shah J, Discrimination of Arabidopsis PAD4 activities in defense against green peach aphid and pathogens. Plant Physiol 158:1860–1872 (2012).
Atamian HS, Chaudhary R, Cin VD, Bao E, Girke T and Kaloshian I, In planta expression or delivery of potato aphid Macrosiphum euphorbiae effectors Me10 and Me23 enhances aphid fecundity. Mol Plant Microbe Interact 26:67–74 (2013).
Elzinga DA and Jander G, The role of protein effectors in plant‐aphid interactions. Curr Opin Plant Biol 16:451–456 (2013).
Pitino M and Hogenhout SA, Aphid protein effectors promote aphid colonization in a plant species‐specific manner. Mol Plant Microbe Interact 26:130–139 (2013).
Divol F, Vilaine F, Thibivilliers S, Amselem J, Palauqui JC, Kusiak C et al., Systemic response to aphid infestation by Myzus persicae in the phloem of Apium graveolens. Plant Mol Biol 57:517–540 (2005).
Park SJ, Huang Y and Ayoubi P, Identification of expression profiles of sorghum genes in response to greenbug phloem‐feeding using cDNA subtraction and microarray analysis. Planta 223:932–947 (2006).
Lemoine R, La Camera S, Atanassova R, Dédaldéchamp F, Allario T, Pourtau N et al., Source‐to‐sink transport of sugar and regulation by environmental factors. Front Plant Sci 4:272 (2013).
Havaux M, Carotenoid oxidation products as stress signals in plants. Plant J 79:597–606 (2014).
Saga Y, Yoshida N, Yamada S, Mizoguchi T and Tamiaki H, Biosynthesis of unnatural glycolipids possessing diyne moiety in the acyl chain in the green sulfur photosynthetic bacterium Chlorobaculum tepidum grown by supplementation of 10,12‐heptadecadiynic acid. Biochem Biophys Rep 9:42–46 (2017).
Novakova E and Moran NA, Diversification of genes for carotenoid biosynthesis in aphids following an ancient transfer from a fungus. Mol Biol Evol 29:313–323 (2012).
Gao J, Guo H, Sun Y and Ge F, Differential accumulation of leucine and methionine in red and green pea aphids leads to different fecundity in response to nitrogen fertilization. Pest Manag Sci 74:1779–1789 (2018).
Yan H, Guo HG, Sun Y and Ge F, Plant phenolics mediated bottom‐up effects of elevated CO2 on Acyrthosiphon pisum and its parasitoid Aphidius avenae. Insect Sci 27:170–184 (2020).
Harlow CD and Lampert EP, Resistance mechanisms in two color forms of the tobacco aphid (Homoptera: Aphididae). J Econ Entomol 83:2130–2135 (1990).
Kerns DL, Palumbo JC and Byrne DN, Relative susceptibility of red and green color forms of green peach aphid to insecticides. Southwest Entomol 23:17–24 (1998).
Schuett W, Dall SRX, Kloesener MH, Baeumer J, Beinlich F and Eggers T, Life‐history trade‐offs mediate ‘personality’ variation in two colour morphs of the pea aphid, Acyrthosiphon pisum. J Animal Ecol 84:90–101 (2015).
Sadowski RA, Nicotine‐induced inhibition of lycopene cyclization in Phaseolus vulgaris cotyledons. Biochem Biophys Res Commun 120:625–630 (1984).
Ishikawa E and Abe H, Lycopene accumulation and cyclic carotenoid deficiency in heterotrophic Chlorella treated with nicotine. J Ind Microbiol Biotechnol 31:585–589 (2004).
Devine GJ, Harling ZK, Scarr AW and Devonshire AL, Lethal and sublethal effects of imidacloprid on nicotine‐tolerant Myzus nicotianae and Myzus persicae. Pestic Sci 48:57–62 (1996).
Nauen R, Strobel J, Tietjen K, Otsu Y, Erdelen C and Elbert A, Aphicidal activity of imidacloprid against a tobacco feeding strain of Myzus persicae (Homoptera: Aphididae) from Japan closely related to Myzus nicotianae and highly resistant to carbamates and organophosphates. Bull Entomol Res 86:165–171 (1996).
Qin G, Gu H, Ma L, Peng Y, Deng XW, Chen Z et al., Disruption of phytoene desaturase gene results in albino and dwarf phenotypes in arabidopsis by impairing chlorophyll, carotenoid, and gibberellin biosynthesis. Cell Res 17:471–482 (2007).
Harris D, Tal O, Jallet D, Wilson A, Kirilovsky D and Adir N, Orange carotenoid protein burrows into the phycobilisome to provide photoprotection. Proc Natl Acad Sci USA 113:1655–1662 (2016).
Squires AH, Dahlberg PD, Liu H, Magdaong NCM, Blankenship RE and Moerner WE, Single‐molecule trapping and spectroscopy reveals photophysical heterogeneity of phycobilisomes quenched by orange carotenoid protein. Nat Commun 10:1172 (2019).
Jiao S, Hilaire E, Paulsen AQ and Guikema JA, Brassica rapa plants adapted to microgravity with reduced photosystem I and its photochemical activity. Physiol Plant 122:281–290 (2004).
Song X, Diao J, Ji J, Wang G, Li Z, Wu J et al., Overexpression of lycopene ε‐cyclase gene from lycium chinense confers tolerance to chilling stress in Arabidopsis thaliana. Gene 576:395–403 (2016).
Frank HA and Cogdell RJ, Carotenoids in photosynthesis. Photochem Photobiol 63:257–264 (1996).
Gao LL, Klingler JP, Anderson JP, Edwards OR and Singh KB, Characterization of pea aphid resistance in Medicago truncatula. Plant Physiol 146:996–1009 (2008).
Rasool B, McGowan J, Pastok D, Marcus SE, Morris JA, Verrall SR et al., Redox control of aphid resistance through altered cell wall composition and nutritional quality. Plant Physiol 175:259–271 (2017).
Guo H, Gu L, Liu F, Chen F, Ge F and Sun Y, Aphid‐borne viral spread is enhanced by virus‐induced accumulation of plant reactive oxygen species. Plant Physiol 179:143–155 (2019).
Mutti NS, Louis J, Pappan LK, Pappan K, Begum K, Chen MS et al., A protein from the salivary glands of the pea aphid, Acyrthosiphon pisum, is essential in feeding on a host plant. Proc Natl Acad Sci USA 105:9965–9969 (2008).
Carolan JC, Caragea D, Reardon KT, Mutti NS, Dittmer N, Pappan K et al., Predicted effector molecules in the salivary secretome of the pea aphid (Acyrthosiphon pisum): a dual transcriptomic/proteomic approach. J Proteome Res 10:1505–1518 (2011).
Colombo M, Raposo G and Thery C, Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Ann Rev Cell Dev Biol 30:255–289 (2014).
Chen Y, Singh A, Kaithakottil GG, Mathers TC, Gravino M, Mugford ST et al., An aphid RNA transcript migrates systemically within plants and is a virulence factor. Proc Natl Acad Sci USA 117:12763–12771 (2020).
Valmalette JC, Dombrovsky A, Brat P, Mertz C, Capovilla M and Robichon A, Light‐induced electron transfer and ATP synthesis in a carotene synthesizing insect. Sci Rep 2:579 (2012).
Tjallingii WF, Regulation of phloem sap feeding by aphids, in Regulatory Mechanisms in Insect Feeding. Springer, Boston, MA, pp. 190–209 (1995).
Tjallingii W and Hogen‐Esch T, Fine structure of aphid stylet routes in plant tissues in correlation with EPG signals. Physiol Entomol 18:317–328 (1993).
Lei J, Finlayson SA, Salzman RA, Shan L and Zhu‐Salzman K, Botrytis‐induced kinase1 modulates Arabidopsis resistance to green peach aphids via phytoalexin deficient 4. Plant Physiol 165:1657–1670 (2014).
Nisbet AJ, Woodford JAT and Strang RHC, Quantifying aphid feeding on non‐radioactive food sources. Entomol Exp Appl 72:85–89 (1994).
Kim JH and Jander G, Myzus persicae (green peach aphid) feeding on Arabidopsis induces the formation of a deterrent indole glucosinolate. Plant J 49:1008–1019 (2007).
Ye J, Qu J, Zhang JF, Geng YF and Fang RX, A critical domain of the cucumber mosaic virus 2b protein for RNA silencing suppressor activity. FEBS Lett 583:101–106 (2009).
Lei R, Du Z, Qiu Y and Zhu S, The detection of hydrogen peroxide involved in plant virus infection by fluorescence spectroscopy. Luminescence 31:1158–1165 (2016).

110202201017(LS-01) Major Special Projects For Green Pest Control; 2022YFD1400800 the National Key R&D Program of China; 32072426and32372636 the National Natural Science Foundation of China

Keywords: Myzus persicae; carotenoid desaturase; color morph; phloem feeding; photosynthesis

EC 1.- (Oxidoreductases)
EC 1.14.99.- (phytoene dehydrogenase)
0 (Insect Proteins)
36-88-4 (Carotenoids)

Date Created: 20240607 Date Completed: 20241011 Latest Revision: 20241011

20241012

10.1002/ps.8225

38847471