МОЛЕКУЛЯРНЫЕ АСПЕКТЫ ИММУНИТЕТА РАСТЕНИЙ И ИХ КОЭВОЛЮЦИИ С НАСЕКОМЫМИ

А.В. Конарев

Аннотация


Огромное разнообразие растений и насекомых является результатом их коэволюции на протяжении сотен миллионов лет. Необходимость защиты тканей и органов, а также хранящихся в них энергетических и пластических материалов от фитофагов привела у растений к появлению многообразных и изощренных механизмов иммунитета. Наличие сложнейших поведенческих реакций, в том числе способности к выбору кормового растения по биохимическим, морфологическим и иным признакам и высокоорганизованной пищеварительной системы, и многие другие особенности насекомых-фитофагов обусловили у растений формирование механизмов иммунитета, в значительной мере независимых от механизмов иммунитета к фитопатогенным микроорганизмам. При этом защитные реакции растений против вредителей и патогенов могут быть сходными на молекулярном уровне передачи сигнала и запуска ответных реакций. Задействованные при этом гормональные системы могут взаимодействовать в антагонистической или синергетической манере, а фитофаги – как микроорганизмы, так и насекомые – способны с помощью эффекторов встраиваться в это взаимодействие для своей выгоды. Очень важна химическая составляющая защитных систем растений, охватывающая практически все классы вторичных метаболитов, которые оказывают прямое токсическое, репеллентное, антипитательное или иное негативное воздействие на фитофагов или привлекают энтомофагов. Широк перечень механизмов их действия – от разрушения клеточных мембран до повышения затрат энергии и ресурсов на усвоение пищи. Разнообразны и механизмы обезвреживания защитных соединений растений насекомыми. В природной системе «растение-насекомое» каждый из ее элементов представляет собой сообщество разнообразных организмов. Симбионты, паразиты и патогены влияют на взаимодействие растений и насекомых и вовлечены в их коэволюцию. При создании форм растений, устойчивых к вредителям, важно учитывать возможные последствия применения того или иного защитного механизма в отношении не только отдельных особей, но также популяций вредителей и агроэкосистемы в целом. Использование механизмов, не стимулирующих ускоренную микроэволюцию вредителей, оказывает более щадящее воздействие на экосистему. В роли таких защитных факторов могут выступать, например, белковые ингибиторы пищеварительных ферментов насекомых. Понимание закономерностей коэволюции растений и насекомых и молекулярной природы адаптации фитофагов к защитным соединениям является необходимым условием для создания эффективных форм растений, устойчивых к вредителям.

Ключевые слова


иммунитет растений к насекомым, коэволюция растений и насекомых, протеиназы, α-амилазы, ингибиторы.

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Литература


Вилкова НА, Нефедова ЛИ, Фролов АН. Иммунитет семенных растений и его фитосанитарное значение в агроэкосистемах. Защита и карантин растений. 2015;(8):3-9.

Вилкова НА. Иммунитет растений к вредным организмам и его биоценотическое значение в стабилизации агроэкосистем и повышении устойчивости растениеводства. Вестник защиты растений. 2000;(2):3-15.

Вилкова НА, Конарев АВ. Современные проблемы иммунитета растений к вредителям. Вестник защиты растений. 2010;(3):3-15.

Долгих ВВ, Сендерский ИВ, Конарев АВ. Получение и свойства рекомбинантных протеиназ Eurygaster integriceps Put., гидролизующих глютенин. Приклад биохимия и микробиол. 2014;50(5):466-74.

Долгих ВВ, Сендерский ИВ, Павлова ОА, Наумов АМ. Уникальные особенности энергетического обмена микроспоридий как результат длительной адаптации к внутриклеточному развитию. Паразитология. 2011;42(5):147-57.

Конарев АВ. Компонентный состав и генетический контроль ингибиторов α-амилаз насекомых из зерна пшениц и эгилопсов. Докл ВАСХНИЛ. 1982;(6):42-4.

Конарев АВ. Методы анализа компонентного состава ингибиторов .-амилаз и протеиназ у злаков. Приклад биохимия и микробиол. 1985; 21(1):92-100.

Конарев АВ. Системы ингибиторов гидролаз у злаков – организация, функции и эволюционная изменчивость. Автореф дисс докт биол наук. М.: Институт биохимии им А.Н. Баха; 1992.

Кузнецова СС, Колесанова ЕФ, Таланова АВ, Веселовский АВ. Перспективы создания новых ингибиторов терапевтически значимых сериновых протеаз на основе кноттинов и пептидного ингибитора трипсина из семян подсолнечника (SFTI 1). Биомед хим. 2016;62(4):353-68.

Максимов ИВ, Сорокань АВ, Нафикова АР, Беньковская ГВ. Возможность и механизмы действия Bacillus subtilis 26Д и Beauveria bassiana Уфа-2 при применении для защиты растений картофеля от фитофтороза и колорадского жука. Микол фитопатол. 2015;49(5):317-24.

Мосолов ВВ, Валуева ТА Ингибиторы протеиназ в биотехнологии растений (обзор). Приклад биохим микробиол. 2008;44(3): 261-9.

Павлюшин ВА, Вилкова НА, Сухорученко ГИ, Фасулати СР, Нефедова ЛИ. Фитосанитарные последствия антропогенной трансформации агроэкосистем. Вестник защиты растений. 2008;(3):3-26.

Рукавцова ЕБ, Алексеева ВВ, Бурьянов ЯИ. Применение РНК-интерференции в метаболической инженерии растений (обзорная статья). Биоорг хим. 2010;36:159-69.

Шафикова ТН, Омеличкина ЮВ. Молекулярно-генетические аспекты иммунитета растений к фитопатогенным бактериям и грибам. Физиология растений. 2015;62:611-27.

Шеленга ТВ, Конарев АВ, Дзюбенко НИ. Эндофитные грибы рода Neotyphodium – выявление и идентификация у овсяницы луговой (Festuca pratensis Huds.). Методические рекомендации. Санкт-Петербург: ВИР; 2007.

Шеленга ТВ, Конарев АВ, Дзюбенко НИ, Малышев ЛЛ, Такаи Т. Изучение образцов овсяницы луговой из коллекции ВИР, содержащих симбиотические грибы-эндофиты рода Neotyphodium. Докл РАСХН. 2006;(1):20-2.

Vilkova NA, Nefedova LI, Frolov AN. [Immunity of seed plants and its phytosanitary value in agroecosystems]. Zaschita i Karantin Rasteniy.2015;(8):3-9. (In Russ.)

Vilkova NA. [Plant immunity against pest organisms and its role in stabilizing agroecosystems and plant growing]. Vestnik Zaschity Rasteniy. 2000;(2):3-15. (In Russ.)

Vilkova NA, Konarev AV. [Modern problems of plant immunity to pests]. Vestnik Zaschity rasteniy. 2010;(3):3-15. (In Russ.)

Dolgikh VV, Senderskiy IV, Konarev AV. Production and properties of recombinant glutenin-hydrolyzing proteinases from Eurygaster integriceps Put. Appl Biochem Microbiol. 2014;50(5):433-40. (English translation of Prikl Biokh Mikr.)

Dolgikh VV, Senderskii IV, Pavlova OA, Naumov AM. [Unique characteristics of the energy metabolism in Microsporidia as a result of durational adaptation to the intracellular development]. Parazitologiya. 2010;45(2):147-57.

Konarev AV. Component composition and genetic control of insect alpha-amylase inhibitors from wheat and Aegilops grain. Soviet Agricultural Science. 1982;(6):68-71. (English Translation of Dokl VASKhNIL)

Konarev AV. [Methods for analyzing the composition of cereal .-amylase and proteinase inhibitors]. Prikl Biokh Mikrobiol. 1985;21(1):92-100. (In Russ.)

Konarev AV. [Systems of hydrolase inhibitors in cereals: organization, functions and evolutionary variability. DSc Thesis]. Moscow: AN Bach Institute of Biochemistry; 1992. (In Russ.)

Kuznetsova SS, Kolesanova EF, Talanova AV, Veselovsky AV. [Prospects for the design of new therapeutically significant protease inhibitors based on knottins and sunflower seed trypsin inhibitor (SFTI 1)]. Biomed Khim. 2016;62(4):353-68. (In Russ.)

Maksimov IV, Sorokan AV, Nafikova AR, Benkovskaya GV. [On the in principle ability and mechanisms of action of the concerted use of Bacillus subtilis 26D and Beauveria Bassiana Ufa-2 preparations for potato protection against Phytophthora Infestans and Leptinotarsa decemlineata]. Mikologiya i Fitopatologiya. 2015;49(5):317-24. (In Russ.)

Mosolov VV, Valueva TA. Proteinase inhibitors in plant biotechnology: A review. Appl Biochem Microbiol. 2008;44(3):233-40. (English Translation of Prikl Biokh Mikr. 2008;44(3):261-9)

Pavlyushin VA, Vilkova NA, Sukhoruchenko GI, Fasulati SR, Nefedova LI. [Phytosanitary consequences of anthropogenic transformation of agricultural ecosystems]. Vestnik Zaschity Rasteniy. 2008;(3):3-26. (In Russ.)

Rukavtsova EB, Alekseyeva VV, Buryanov YaI. The use of RNA interference for the metabolic engineering of plants (review). Russ J Bioorganic Chem. 2010;36(2):146-56. (English translation of Bioorg Chem. 2010;36(2):159-69). 95

Shafikova TN, Omelichkina YV. Molecular genetic aspects of plant immunity to phytopathogenic bacteria and fungi. Russ J Plant Physiol. 2015;62(5):571-85. (English translation of Fiziol Rast. 2015;62(5):611-27).

Shelenga TV, Konarev AV, Dzubenko NI. Endofitnye Griby Roda Neotyphodium – Vyavleniye i Identifikatsiya u Ovsianitsy Lugovoy (Festuca pratensis Huds.) Metodicheskiye Rekomendatsii. [Endophyte Fungi of Genus Neotyphodium: Detection and Identification in Meadow Fescue (Festuca pratensis Huds.) Methodological Guide]. Saint Petersburg: VIR; 2007. (In Russ.)

Shelenga TV, Konarev AV, Dzubenko NI, Malyshev LL, Takai T. [Study of meadow fescue (Festuca pratensis Huds.) accessions (from N.V.Vavilov institute collection) containing the endophyte fungi of genus Neotyphodium (=Acremonium)]. Dokl RASKhN, 2006;(1):20-2. (In Russ.)

Acevedo FE, Rivera-Vega LJ, Chung SH, Ray S, Felton GW. Cues from chewing insects – the intersection of DAMPs, HAMPs, MAMPs and effectors. Curr Opin Plant Biol. 2015;26:80-6.

Ahn JE, Zhu-Salzman K. CmCatD, a cathepsin D-like protease has a potential role in insect defense against a phytocystatin. J Insect Physiol. 2009;55:678-85.

Amirhusin B, Shade RE, Koiwa H, Hasegawa PM, Bressan RA, Murdock LL, Zhu-Salzman K. Soyacystatin N inhibits proteolysis of wheat .-amylase inhibitor and potentiates toxicity against cowpea weevil. Econ Entomol. 2004;97:2095-100.

Amiri A, Bandani AR, Alizadeh H. Molecular identification of cysteine and trypsin protease effect of different hosts on protease expression, and RNAi mediated silencing of cysteine protease gene in the Sunn pest. Arch Insect Biochem Physiol. 2016;91(4):189-209.

Bateman KS, James MN. Plant protein proteinase inhibitors: structure and mechanism of inhibition. Curr Protein Pept Sci. 2011;12(5):340-7.

Becerra JX. On the factors that promote the diversity of herbivorous insects and plants in tropical forests. Proc Natl Acad Sci USA. 2015;112(19):6098103.

Berkut AA, Usmanova DR, Peigneur S, Oparin PB, Mineev KS, Odintsova TI, Tytgat J, Arseniev AS, Grishin EV, Vassilevski AA. Structural similarity between defense peptide from wheat and scorpion neurotoxin permits rational functional design. J Biol Chem. 2014;289:14331-40.

Bhat NS, Puttarangappa, Virupakshappa K, Prasad DT. Proteinase inhibitor in sunflower seed and its influence on growth and development of capitulum borer Helicoverpa armigera (Hubner). In:

Blair MW, Munoz C, Buendia HF, Flower J, Bueno JM, Cardona C. Genetic mapping of microsatellite markers around the arcelin bruchid resistance locus in common bean. Theor Appl Genet. 2010;121:393-402.

Brar DS, Virk PS, Jena KK, Khush GS. Breeding for resistance to planthoppers in rice. In: Heong KL and Hardy B, eds. Plant hoppers: new threats to the sustainability of intensive rice production systems in Asia. Los Banos: International Rice Research Institute; 2009. p. 401-9.

Broadway RM. The response of insects to dietary protease inhibitors. In: Michaud D, ed. Recombinant Protease Inhibitors in Plants. Landes Bioscience; 2000. p. 80-8.

Celorio-Mancera MP, Greve LC, Teuber LR, Labavitch JM. Identification of endo-and exo-polygalacturonase activity in Lygus hesperus Knight salivary glands. Arch Insect Biochem Physiol. 2009;70(2):122-35.

Chan LY, Craik DJ, Daly NL. Dual-targeting anti-angiogenic cyclic peptides as potential drug leads for cancer therapy. Sci Rep. 2016;6:35347.

Chen W, Kinsler VA, Macmillan D, Di WL. Tissue kallikrein inhibitors based on the sunflower trypsin inhibitor scaffold – a potential therapeutic intervention for skin diseases. PLoS One. 2016;11(11):e0166268. http://dx.doi.org/10.1371/ journal.pone.0166268

Clemente A, Arques MC. Bowman-Birk inhibitors from legumes as colorectal chemopreventive agents. World J Gastroenterol. 2014;20:10305-15.

Coaker G. Plant-pathogen effectors: Cellular probes interfering with plant defenses in spatial and temporal manners. Annu Rev Phytopathol. 2016;54:419-41.

Conners R, Konarev AV, Forsyth J, Lovegrove A, Marsh J, Joseph-Horne T, Shewry PR, Brady RL. An unusual helix-turn-helix protease inhibitory motif in a novel trypsin inhibitor from seeds of Veronica (Veronica hederifolia L.). J Biol Chem. 2007;282:27760-8.

de Andrade EC, Hunter WB. RNA interference – natural gene-based technology for highly specific pest control (HiSPeC). In: Abdurakhmonov IY, ed. RNA Interference. InTech; 2016. http://dx.doi.org/10.5772/61612.

de Oliveira CFR, de Moura MC, Napoleao TH, Paiva PMG, Coelho LCBB, Macedo MLR. A chitin-binding lectin from Moringa oleifera seeds (WSMoL) impairs the digestive physiology of the Mediterranean flour larvae, Anagasta kuehniella. Pestic Biochem Physiol. 2017: http://dx.doi.org/10.1016/j.pestbp.2017.01.006

Despres L, David JP, Gallet C. The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol. Evol. 2007;22:298-307.

Dobler S, Dalla S, Wagschal V, Agrawal AA. Community-wide convergent evolution in insectadaptation to toxic cardenolides by substitutions in the Na,K-ATPase. Proc Natl Acad Sci USA. 2012;109:13040-5.

D’Ovidio R, Raiola A, Capodicasa C, Devoto A, Pontiggia D, Roberti S, Galletti R, Conti E, O’Sullivan D, De Lorenzo G. Characterization of the complex locus of bean encoding polygalacturonase-inhibiting proteins reveals subfunctionalization for defense against fungi and insects. Plant Physiol. 2004;135:2424-35.

Dunaevsky YE, Elpidina EN, Vinokurov KS, Belozersky MA. Protease inhibitors in improvement of plant resistance to pathogens and insects. Mol Biol.2005;39(4):608-13.

Elliott AG, Franke B, Armstrong DA, Craik DJ, Mylne JS, Rosengren KJ. Natural structural diversity within a conserved cyclic peptide scaffold. Amino Acids. 2016. http://dx.doi.org/10.1007/s00726-016-2333-x

Elliott AG, Delay C, Liu H, Phua Z, Rosengren KJ, Benfield AH, Panero JL, Colgrave ML, Jayasena AS, Dunse KM, Anderson MA, Schilling EE, Ortiz-Barrientos D, Craik DJ, Mylne JS. Evolutionary origins of a bioactive peptide buried within preproalbumin. Plant Cell. 2014;26:981-95.

Emebiri LC, Tan MK, El-Bouhssini M, Wildman O, Jighly A, Tadesse W, Ogbonnaya FC. QTL mapping identifies a major locus for resistance in wheat to Sunn pest (Eurygaster integriceps) feeding at the vegetative growth stage. Theor Appl Genet. 2016. http://dx.doi.org/10.1007/s00122-0162812-1.

Every D, Sutton KH, Shewry PR, Tatham AS, Coolbear T. Specificity of action of an insect proteinase purified from wheat grain infested by the New Zealand wheat bug, Nysius huttoni. J Cereal Sci. 2005;42(2):185-91.

Fakhoury AM, Woloshuk CP. Inhibition of growth of Aspergillus flavus and fungal alpha-amylases by a lectin-like protein. Mol Plant-Microbe Interact. 2001;14:955-61.

Fatehi F, Behamta MR, Zali AA. Evaluating the resistance to sunn pest (Eurygaster integriceps Put) and its relationship with high-molecularweight glutenin subunit in wheat. In: Proc. 11th Int Wheat Genet Symp, Brisbane, Australia, Vol. 3. Sydney: University Press; 2008. p. 741-3.

Ferrari S, Galletti R, Pontiggia D, Manfredini C, Lionetti V, Bellincampi D, Cervone F, De Lorenzo G. Transgenic expression of a fungal Proc. 14th International Sunflower Conf. Beijing/ Shenyang; 1996. p. 523-32.

Fire AZ. Gene silencing by double.stranded RNA (Nobel lecture). Angew Chem Int Ed 2007;46:6966-84.

Franco OL, Rigden DJ, Melo FR, Grossi.de.Sa MF. Plant ..amylase inhibitors and their interaction with insect ..amylases. Eur J Biochem 2002;269:397-412.

Frati F, Galletti R, De Lorenzo G, Salerno G, Conti E. Activity of endo-polygalacturonases in mirid bugs (Heteroptera: Miridae) and their inhibition by plant cell wall proteins (PGIPs). Eur J Entomol. 2006;103:515-22.

Furch AC, van Bel AJ, Will T. Aphid salivary proteases are capable of degrading sieve-tube proteins. J Exp Bot. 2015;66:533-9.

Gatehouse JA. Prospects for using proteinase inhibitors to protect transgenic plants against attack by herbivorous insects. Curr Protein Pept Sci. 2011;12(5):409-16.

Grossi de Sa MF, Mirkov TE, Ishimoto M, Colucci G, Bateman KS, Chrispeels MJ. Molecular characterization of a bean .-amylase inhibitor that inhibits the .-amylase of the Mexican bean weevil Zabrotes subfasciatus. Planta. 1997;203:295-303.

Grossi-de-Sa MF, Pelegrini PB, Vasconcelos IM, Carlini CR, Silva MS. Entomotoxic plant proteins: potential molecules to develop genetically modified plants resistant to insect-pests. In: Gopalakrishnakone P, ed. Plant Toxins. Toxinology. Dordrecht: Springer Science; 2015. http://dx.doi.org/10.1007/978-94-007-6728-7_13-1

Hammer TJ, Bowers MD. Gut microbes may facilitate insect herbivory of chemically defended plants. Oecologia. 2015;179:1-14.

Hansen AK, Moran NA. The impact of microbial symbionts on host plant utilization by herbivorous insects. Mol Ecol. 2014;23:1473-96.

Heidel-Fischer HM, Vogel H. Molecular mechanisms of insect adaptation to plant secondary compounds. Curr Opin Insect Sci. 2015;8:8-14.

Heinrich M. Has plant-insect coevolution had an impact on the human brain? BioScience. 2015.65(1):104-5.

Howe GA, Jander G. Plant immunity to insect herbivores. Annu Rev Plant Biol. 2008;59:41-66.

Hui DQ, Iqbal J, Lehmann K, Gase K, Saluz HP, Baldwin IT. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. V. Microarray analysis and further characterization of large-scale changes in herbivore-induced mRNAs. Plant Physiol. 2003;131(4):1877-93. 97

Jamal F, Pandey PK, Singh D, Khan MY. Serine protease inhibitors in plants: nature’s arsenal crafted for insect predators. Phytochem Rev. 2013;12(1):1-34.

Jendrny C, Beck-Sickinger AG. Inhibition of kallikrein-related peptidases 7 and 5 by grafting serpin reactive-center loop sequences onto sunflower trypsin inhibitor-1 (SFTI-1). ChemBioChem. 2016;17:719-26.

Jongsma M, Beekwilder J. Co-evolution of insect proteases and plant protease inhibitors. Curr Protein Pept Sci. 2011;12:437-47.

Kaur R, Gupta AK. Insect amylase-plant amylase inhibitor interaction is key to success of transgenics against insect herbivory. Biochem Anal Biochem. 2015;4(4):1. http://dx.doi.org/10.4172/21611009.1000201

Kennedy DO. Plants and the Human Brain. Oxford University Press; 2014.

Kessler A, Baldwin IT. Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol. 2002;53:299-328.

Kessler A, Halitschke R, Baldwin IT. Silencing the jasmonate cascade: induced plant defenses and insect populations. Science. 2004;305:665-8.

Kim J, Quaghebeur H, Felton GW. Reiterative and interruptive signaling in induced plant resistance to chewing insects. Phytochemistry. 2011;72:1624-34.

Konarev AV. Interaction of insect digestive enzymes with plant protein inhibitors and host-parasite coevolution. Euphytica. 1996;92:89-94.

Konarev AV, Anisimova IN, Gavrilova VA, Rozhkova VT, Fido R, Tatham AS, Shewry PR. Novel proteinase inhibitors in seeds of sunflower (Helianthus annuus L.): polymorphism, inheritance and properties . Theor Appl Genet. 2000;100:82-8.

Konarev AV, Anisimova IN, Gavrilova VA, Shewry PR. Polymorphism of inhibitors of hydrolytic enzymes present in cereal and sunflower seeds. In: Mugnozza GTS, Porceddu E, Pagnotta MA, eds. Genetics and Breeding for Crop Quality and Resistance: Proc. XV EUCARPIA Congress, Viterbo, Italy, September 20–25, 1998. Springer Netherlands; 1999. p.135-44. http://dx.doi.org/10.1007/978-94-011-4475-9_16

Konarev AV, Anisimova IN, Gavrilova VA, Vachrusheva TE, Konechnaya GY, Lewis M, Shewry PR. Serine proteinase inhibitors in the Compositae: distribution, polymorphism and properties. Phytochemistry. 2002;59:279-91.

Konarev AV, Beaudoin F, Marsh J, Vilkova NA, Nefedova LI, Sivr D, Koksel H, Shewry PR, Lovegrove A. Characterization of a glutenin-specific serine proteinase of sunn bug Eurygaster integricepts Puton. J Agric Food Chem. 2011;59(6):2462-70. endo-polygalacturonase increases plant resistance to pathogens and reduces auxin sensitivity. Plant Physiol. 2008;146:669-81.

Konarev AV, Griffin J, Konechnaya GY, Shewry PR. The distribution of serine proteinase inhibitors in seeds of the Asteridae. Phytochemistry. 2004;65:3003-20.

Konarev AV, Lovegrove A. Novel detection methods used in conjunction with affinity chromatography for the identification and purification of hydrolytic enzymes or enzyme inhibitors from insects and plants. In: Magdeldin S, ed. Affinity Chromatography. InTech; 2012. p. 187-210. http://dx.doi.org/10.5772/37618

Konarev AV, Lovegrove A, Shewry PR. Serine proteinase inhibitors in seeds of Cycas siamensis and other gymnosperms. Phytochemistry. 2008;69:2482-9.

Konarev AV, Tomooka N, Ishimoto M, Vaughan D. Variability of the inhibitors of serine, cysteine proteinases and insect .-amylases in Vigna and Phaseolus. In: Mugnozza GTS, Porceddu E, Pagnotta MA, eds. Genetics and Breeding for Crop Quality and Resistance: Proc. XV Eucarpia Congress, Viterbo, Italy, September 20-25, 1998. Springer Netherlands;1999. p. 173-81. http://dx.doi.org/10.1007/978-94-011-4475-9_20

Li F, Yang XX, Xia HC, Zeng R, Hu WG, Li Z, Zhang ZC. Purification and characterization of Luffin P1, a ribosome-inactivating peptide from the seeds of Luffa cylindrica. Peptides. 2003;24:799805.

Luan JB, Chen W, Hasegawa DK, Simmons AM, Wintermantel WM, Ling KS, Fei Z, Liu S-Sh, Douglas AE. Metabolic coevolution in the bacterial symbiosis of whiteflies and related plant sap-feeding insects. Genome Biol Evol. 2015;7:2635-47.

Luckett S, Garcia RS, Barker JJ, Konarev AV, Shewry PR, Clarke AR, Brady RL. Highresolution structure of a potent, cyclic proteinase inhibitor from sunflower seeds. J Mol Biol. 1999;290:525-33.

Macedo MR, Freire MGM. Insect digestive enzymes as a target for pest control. Invert Surviv J. 2011;8:190-8.

Marcus JP, Green JL, Goulter KC, Manners JM. A family of antimicrobial peptides is produced by processing of a 7S globulin protein in Macadamia integrifolia kernels. Plant J. 1999;19:699-710.

Maulik A, Sarkar AI, Devi S, Basu S. Polygalacturonase.inhibiting proteins-leucine.rich repeat proteins in plant defense. Plant Biology. 2012;14(Suppl 1):22-30.

McHale L, Tan X, Koehl P, Michelmore RW. Plant NBS-LRR proteins: adaptable guards. Genome Biol. 2006;7(4):article 212.

Mehrabadi M, Bandani AR, Franco OL. Plant proteinaceous alpha-amylase and proteinase inhibitors and their use in insect pest control. New Perspectives in Plant Protection. InTech; 2012. http:// dx.doi.org/10.5772/39290.

Mewis I, Appel HM, Hom A, Raina R, Schultz JC. Major signaling pathways modulate Arabidopsis glucosinolate accumulation and response to both phloem-feeding and chewing insects. Plant Physiol. 2005;138:1149-62.

Mithofer A, Boland W. Plant defense against herbivores: chemical aspects. Annu Rev Plant Biol. 2012;63:431-50.

Musser RO, Hum-Musser SM, Eichenseer H, Peiffer M, Ervin G, Murphy JB, Felton GW. Herbivory: Caterpillar saliva beats plant defenses – a new weapon emerges in the evolutionary arms race between plants and herbivores. Nature. 2002;416:599-600.

Nakasu EY, Edwards MG, Fitches E, Gatehouse JA, Gatehouse AM. Transgenic plants expressing .-ACTX-Hv1a and snowdrop lectin (GNA) fusion protein show enhanced resistance to aphids. Front Plant Sci. 2014;5:673. http://dx.doi.org/10.3389/ fpls.2014.00673.

Northfield SE, Wang CK, Schroeder CI, Durek T, Kan MW, Swedberg JE, Craik DJ. Disulfide-rich macrocyclic peptides as templates in drug design. Eur J Med Chem. 2014;77:248-57.

Oliveira AS, Xavier-Filho J, Sales MP. Cysteine proteinases and cystatins. Braz Arch Biol Technol. 2003;46:91-104.

Oparin PB, Mineev KS, Dunaevsky YE, Arseniev AS, Belozersky MA, Grishin EV, Egorov TA, Vassilevski AA. Buckwheat trypsin inhibitor with helical hairpin structure belongs to a new family of plant defence peptides. Biochem J. 2012;446:69-77.

Oppert B, Morgan TD, Culbertson C, Kramer KJ. Dietary mixtures of cysteine and serine proteinase-inhibitors exhibit synergistic toxicity toward the red flour beetle, Tribolium castaneum. Comp Biochem Physiol. 1993;105:379-85.

Orona.Tamayo D, Wielsch N., Blanco.Labra A, Svatos A, Farias.Rodriguez R, Heil M. Exclusive rewards in mutualisms: ant proteases and plant protease inhibitors create a lock-key system to protect Acacia food bodies from exploitation. Mol Ecol. 2013;22:4087-100.

Ostergaard H, Rasmussen SK, Roberts TH, Hejgaard J. Inhibitory serpins from wheat grain with reactive centers resembling glutamine-rich repeats of prolamin storage proteins. Cloning and characterization of five major molecular forms. J Biol Chem. 2000;275:33272-9.

Palle SR, Campbell LM, Pandeya D, Puckhaber L, Tollack LK, Marcel S, Sundaram S, Stipanovic RD, Wedegaertner TC, Hinze L, Rathore KS. RNAi.mediated ultra.low gossypol cottonseed trait: performance of transgenic lines under field conditions. Plant Biotechnol J. 2013;11:296304.

Pandey D, Rajendran SRCK, Gaur M, Sajeesh PK, Kumar A. Plant defense signaling and responses against necrotrophic fungal pathogens. J. Plant Growth Regul. 2016;35:1159-74.

Park CS, Miller C. Mapping function to structure in a channel-blocking peptide: electrostatic mutants of charybdotoxin. Biochemistry. 1992;31:7749-55.

Petschenka G, Pick C, Wagschal V, Dobler S. Functional evidence for physiological mechanisms to circumvent neurotoxicity of cardenolides in an adapted and a non-adapted hawk-moth species. Proc Biol Sci 2013;280:20123089. DOI: 10.1098/rspb.2012.3089

Poelman EH, Dicke M. Plant.mediated interactions among insects within a community ecological perspective. Annu Plant Rev. 2014;47:309-37.

Popay AJ. Insect pests. In: Fribourg HA, Hannaway DB, West CP, eds. Tall Fescue for the Twenty-first Century. Amer Soc Agron Monograph Series 53; 2009. p. 129-49. http://dx.doi.org/10.2134/agronmonogr53.c9

Powell AL, van Kan J, ten Have A, Visser J, Greve LC, Bennett AB, Labavitch JM. Transgenic expression of pear PGIP in tomato limits fungal colonization. Mol Plant Microbe Interact. 2000;13:942-50.

Qiu Y, Taichi M, Wei N, Yang H, Luo KQ, Tam JP. An orally active bradykinin B1 receptor antagonist engineered as a bifunctional chimera of sunflower trypsin inhibitor. J Med Chem. 2016;60:504-10

Rasoolizadeh A, Munger A, Goulet MC, Sainsbury F, Cloutier C, Michaud D. Functional proteomics-aided selection of protease inhibitors for herbivore insect control. Sci Rep. 2016; 6:38827 http://dx.doi.org/10.1038/srep38827

Ray S, Gaffor I, Acevedo FE, Helms A, Chuang WP, Tooker J, Felton GW, Luthe DS. Maize plants recognize herbivore-associated cues from caterpillar frass. J Chem Ecol. 2015;41:781-92.

Richardson M. Seed storage proteins: the enzyme inhibitors. Meth Plant Biochem. 1991;5:259-305.

Sanchez-Monge R, Gomez L, Garcia-Olmedo F, Salcedo G. New dimeric inhibitor of heterologous .-amylases encoded by a duplicated gene in the short arm of chromosome 3B of wheat (Triticum aestivum L.). Eur J Biochem. 1989;183:37-40. 99

Sanchis V. From microbial sprays to insect-resistant transgenic plants: history of the biospesticide Bacillus thuringiensis. Agron Sustain Dev. 2011;31:217-31.

Schellenberger U, Oral J, Rosen BA, Wei JZ, Zhu G, Xie W, McDonald, MJ, Cerf DC, Diehn SH, Crane VC, Sandahl GA, Zhao J-Z, Nowatzki TM, Sethi A, Liu L, Pan Z, Wang Y, Lu AL, Wu G, Liu L. A selective insecticidal protein from Pseudomonas for controlling corn rootworms. Science. 2016;354(6312):634-7.

Schroeder HE, Gollash S, Moore A. Bean .-amylase-inhibitor confers resistance to the pea weevil (Bruchus pisorum) in transgenic peas (Pisum sativum L). Plant Physiol. 1995;107:1233-9.

Schwachtje J, Minchin PE, Jahnke S, van Dongen JT, Schittko U, Baldwin IT. SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots. Proc Natl Acad Sci USA. 2006;103(34):12935-40.

Shamsi TN, Parveen R, Fatima S. Characterization, biomedical and agricultural applications of protease inhibitors: A review. Int J Biol Macromolec. 2016. http://dx.doi.org/10.1016/j.ijbiomac.2016.02.069

Shelomi M, Danchin EGJ, Heckel DG, Wipfler B, Bradler S, Zhou X, Pauchet Y. Horizontal gene transfer of pectinases from bacteria preceded the diversification of stick and leaf insects. Sci Rep. 2016;6:26388. http://dx.doi.org/10.1038/srep26388

Smith CM, Clement SL. Molecular bases of plant resistance to arthropods. Annu Rev Entomol. 2012;57:309-28.

Spit J, Holtof M, Badisco L, Vergauwen L, Vogel E, Knapen D, Broeck JV. Transcriptional analysis of the adaptive digestive system of the migratory locust in response to plant defensive protease inhibitors. Sci Rep. 2016;6; article 32460. http://dx. doi.org/10.1038/srep32460

Steppuhn A, Baldwin IT. Resistance management in a native plant: Nicotine prevents herbivores from compensating for plant protease inhibitors. Ecol Lett. 2007;10:499-511.

Strauss SY, Rudgers JA, Lau JA, Irwin RE. Direct and ecological costs of resistance to herbivory. Trends Ecol Evol. 2002;17:278-85.

Tabashnik BE, Brevault T, Carriere Y. Insect resistance to Bt crops: lessons from the first billion acres. Nat Biotechnol. 2013;31(6):510-21.

Tanaka A, Tapper BA, Popay A, Parker EJ, Scott B. A symbiosis expressed non.ribosomal peptide synthetase from a mutualistic fungal endophyte of perennial ryegrass confers protection to the symbiotum from insect herbivory. Mol Microbiol. 2005;57(4):1036-50.

Terra WR, Ferreira C. Insect digestive enzymes: properties, compartmentalization and function. Comp Biochem Physiol B Comp Biochem. 1994;109:1-62.

Tetard.Jones C, Edwards R. Potential roles for microbial endophytes in herbicide tolerance in plants. Pest Manag Sci. 2016;72(2):203-9.

Underwood W. Contributions of host cellular trafficking and organization to the outcomes of plant-pathogen interactions. Semin Cell Develop Biol. 2016;56163-73.

Vandenborre G, Smagghe G, Van Damme EJ. Plant lectins as defense proteins against phytophagous insects. Phytochemistry. 2011;72(13):1538-50.

van Eck L, Schultz T, Leach JE, Scofield SR, Peairs FB, Botha AM, Lapitan NL. Virus-induced gene silencing of WRKY53 and an inducible phenylalanine ammonia-lyase in wheat reduces aphid resistance. Plant Biotechnol J. 2010;8(9):1023-32.

Vavra J, Lukes J. Microsporidia and ‘The Art of Living Together’. In: Rollinson D, ed. Advances in Parasitology. Academic Press; 2013. p. 253-320.

Vishram A, Clack B. Identification of prolyl endopeptidase (PEP) inhibitory peptides from Lactobacillus helveticus digestion of four recombinant bovine caseins. FASEB J. 2015;29(Suppl 1):894.12.

Volpicella M, Leoni C, Costanza A, De Leo F, Gallerani R, Ceci LR. Cystatins, serpins and other families of protease inhibitors in plants. Curr Protein Pept Sci. 2011;12:386-98.

Wang LZ, Beuerle T, Timbilla J, Ober D. Independent recruitment of a flavin-dependent monooxygenase for safe accumulation of sequestered pyrrolizidine alkaloids in grasshoppers and moths. PLoS One. 2012;7(2):e31796. http://dx.doi.org/10.1371/journal.pone.0031796

Wang M, Wang L, Chen T, Walker B, Zhou M, Sui D, Conlon JM, Shaw C. Identification and molecular cloning of a novel amphibian Bowman Birk-type trypsin inhibitor from the skin of the Hejiang Odorous Frog; Odorrana hejiangensis. Peptides. 2012;33(2):245-50.

Wato S, Kamei K, Arakawa T, Philo J, Wen J, Hara S, Yamaguchi H. A chimera-like .-amylase inhibitor suggesting the evolution of Phaseolus vulgaris .-amylase inhibitor. J Biochem. 2000;128:139-44.

Werteker M, Kramreither G. Relation between susceptibility to wheat bug attack and digestibility of glutenin. J Cereal Sci. 2008;47:226-32.

Wheat CW, Vogel H, Wittstock U, Braby MF, Underwood D, Mitchell-Olds T. The genetic basis of a plant-insect coevolutionary key innovation. Proc Natl Acad Sci. USA. 2007;104:20427-31.

Wybouw N, Dermauw W, Tirry L, Stevens C, Grbic M, Feyereisen R, Van Leeuwen T. A gene horizontally transferred from bacteria protects arthropods from host plant cyanide poisoning. eLife. 2014;3:e02365. DOI 10.7554/ eLife.02365.001

Yandamuri RC, Gautam R, Darkoh C, Dareddy V, El-Bouhssini M, Clack BA. Cloning, expression, sequence analysis and homology modeling of the prolyl endoprotease from Eurygaster integriceps Puton. Insects. 2014;5:762-82.

Yang LM, Fang ZY, Dicke M, van Loon JA, Jongsma MA. The diamondback moth, Plutella xylostella, specifically inactivates Mustard Trypsin Inhibitor 2 (MTI2) to overcome host plant defence. Insect Biochem Mol Bio. 2009;39:55-61.

Yarullina LG, Akhatova AR, Kasimova RI. Hydrolytic enzymes and their proteinaceous inhibitors in regulation of plant-pathogen interactions. Russ J Plant Physiol. 2016;63(2):193-203.

Yu X, Wang G, Huang S, Ma Y, Xia L. Engineering plants for aphid resistance: current status and future perspectives. Theor Appl Genet. 2014;127:2065-83.

Zhu F, Poelman EH, Dicke M. Insect herbivoreassociated organisms affect plant responses to herbivory. New Phytol. 2014;204:315-21.

Zhu-Salzman K, Zeng R. Insect response to plant defensive protease inhibitors. Annu Rev Entomol. 2015;60:233-52.




DOI: http://dx.doi.org/10.24855/biosfera.v9i1.325

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