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Tolerance in Maize Landraces to Diabrotica Speciosa (Coleoptera: Chrysomelidae) Larvae and Its Relationship to Plant Pigments, Compatible Osmolytes, and Vigor

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Tolerance in Maize Landraces to Diabrotica Speciosa (Coleoptera: Chrysomelidae) Larvae and Its Relationship to Plant Pigments, Compatible Osmolytes, and Vigor applyparastyle "fig//caption/p[1]" parastyle "FigCapt" F&R "All rights reserved. For permissions, please e-mail" (CopyrightLine) "^nAll rights reserved. For permissions, please e-mail" (CopyrightLine) Journal of Economic Entomology, 114(1), 2021, 377–386 doi: 10.1093/jee/toaa292 Advance Access Publication Date: 5 January 2021 Plant Resistance Research Tolerance in Maize Landraces to Diabrotica speciosa (Coleoptera: Chrysomelidae) Larvae and Its Relationship to Plant Pigments, Compatible Osmolytes, and Vigor Eduardo Neves Costa,1,2,5, Bruno Henrique Sardinha de Souza,1,3, 1 4 Zulene Antônio Ribeiro, Durvalina Maria Mathias dos Santos, and Downloaded from https://academic.oup.com/jee/article/114/1/377/6063497 by guest on 28 September 2021 Arlindo Leal Boiça Júnior1 1Faculdade de Ciências Agrárias e Veterinárias, Campus de Jaboticabal, Departamento de Ciências da Produção Agrícola, Universidade Estadual Paulista, 14884-900, Jaboticabal, SP, Brazil, 2Faculdade de Ciências Agrárias, Universidade Federal da Grande Dourados, 79804-970, Dourados, MS, Brazil, 3Departamento de Entomologia, Universidade Federal de Lavras, 37200-000, Lavras, MG, Brazil, 4Faculdade de Ciências Agrárias e Veterinárias, Campus de Jaboticabal, Departamento de Biologia Aplicada à Agropecuária, Universidade Estadual Paulista, 14884-900, Jaboticabal, SP, Brazil, and 5Corresponding author, e-mail: [email protected] Subject Editor: Frank Peairs Received 30 August 2020; Editorial decision 20 November 2020 Abstract The rootworm Diabrotica speciosa (Germar) is native to South America and causes severe economic losses to several crops due to root feeding and disease spread. In maize (Zea mays L.), losses in production come from larval rootworm attack on plant roots resulting in plant health problems, including stalk lodging. More options for controlling this pest are needed to create well balanced, integrated pest management programs for farmers in this region. Natural sources of tolerance in maize genotypes are important for maize breeding programs, and this study investigated the expression of tolerance in several Brazilian maize landraces to D. speciosa. Plant vigor and compounds associated with plant health, including chlorophylls, carotenoids, glycine betaine, and proline were assessed for each landrace. Five landraces and one maize cultivar were selected based on their levels of antibiosis-resistance to D. speciosa that were determined in a prior screening. The percent re- duction in plant growth was used as the measure of tolerance. The landrace Azteca was classified as tolerant to D. speciosa larval feeding, displaying less reduction in plant matter despite having lower plant vigor. This landrace also had higher amounts of chlorophyl and carotenoid pigments, suggesting a positive correlation between tolerance to D. speciosa and higher contents of these photosynthetic pigments. The compatible osmolytes glycine betaine and proline do not seem to be associated with tolerance in maize landraces to D. speciosa larvae. Landrace Azteca seems promising for plant breeding, and repeated field studies are needed to confirm its suitability in maize integrated pest management. Key words: Zea mays L., native resistance, chlorophyl, carotenoids, glycine betaine Tolerance is characterized by the ability of a plant to withstand or Tolerance mechanisms differ from those of antibiosis and recover from injury caused by arthropod pests. Expression of toler- antixenosis. Examples of tolerance mechanisms include increased ance is determined by heritable qualities (plant genotype), allowing photosynthetic activity, compensatory regrowth, utilization of stored the tolerant genotype to withstand injury and regrow (Smith 2005). resources, and phenological changes. Conversely, other resistant From an agronomic perspective, tolerant plant cultivars and hybrids plants are characterized by the presence of morphological and/or produce more biomass and greater yield than susceptible plants chemical traits that adversely affect herbivore performance (anti- when under pest pressure. Furthermore, arthropod populations are biosis) or preference (antixenosis) (Tiffin 2000). Although tolerance not reduced when exposed to tolerant plants, as occurs for plants ex- is important in integrated pest management programs as an integral pressing antibiosis or antixenosis (Smith 2005). Therefore, tolerant determinant of economic injury levels and threshold levels of a crop, plants do not exert selection pressure on herbivore populations, thus it is less often investigated than antixenosis and antibiosis as a source they do not contribute to the emergence of resistant arthropod bio- of crop protection (Peterson et al. 2013, Cruz et al. 2016, Sperotto types (Schoonhoven et al. 2005). et al. 2018). © The Author(s) 2021. Published by Oxford University Press on behalf of Entomological Society of America. 377 All rights reserved. For permissions, please e-mail: [email protected]. 378 Journal of Economic Entomology, 2021, Vol. 114, No. 1 Antibiosis occurs when a plant possesses traits that have adverse and causes economic losses due to larval attack on belowground effects on survival, development, fecundity, or fertility of a potential plant structures including roots and tubers of several crops, including pest arthropod, while antixenosis is characterized by negative effects maize (Viana 2010). The economic impact in agriculture and the re- on arthropod behavior, leading to delayed acceptance and possible sources expended to control this pest in Brazil have not yet been es- outright rejection of a plant as a host (Smith and Clement 2012). timated, although extensive amounts of insecticide active ingredients Some authors suggest that plants invest a lot of energy in the ex- are applied annually to different crops for control of D. speciosa pression of antibiosis (and/or antixenosis) or tolerance, and usually larvae and adults (Ávila and Santana 2011). Although it is poorly one of these strategies prevail over the other as a response to the studied, evolution of resistance of D. speciosa to insecticides has insect attack. (Rosenthal and Kotanen 1994, De Jong and Van Der probably occurred in South America (Cabrera Walsh et al. 2020). Meijden 2000). Attack of D. speciosa larvae has economic importance to maize, As noted above, mechanisms of tolerance often involve changes justifying the need for sustainable pest control tactics. Therefore, this in photosynthesis in injured plants including activation of dor- research aimed to evaluate tolerance in Brazilian maize landraces to mant meristems, changes in plant architecture, partitioning of feeding by D. speciosa larvae. In addition, it was investigated the photoassimilates, source-sink relationships for resource allocation, relationship between tolerance expression, plant vigor, and contents Downloaded from https://academic.oup.com/jee/article/114/1/377/6063497 by guest on 28 September 2021 and greater photosynthetic capacity (Schwachtje and Baldwin 2008, of photosynthetic pigments and compatible osmolytes, which are es- Mitchell et al. 2016). Chlorophyll plays an important role in photo- sential components of plant photosynthesis. synthesis, resulting in greater plant growth and accumulation of dry matter, as well as assisting in plant adaptation to the environment (Engel and Poggiani 1991). Carotenoids are also essential for the Materials and Methods photochemical apparatus. They are important to plant tolerance as antioxidants and phytohormone precursors, e.g., abscisic acid and Numbers of D. speciosa Larvae per Maize Plant anti-stress hormones (Howitt and Pogson 2006). Carotenoids are The experiment was performed in a greenhouse in the Department of accessory pigments in light absorption, transferring energy to the Agricultural Sciences, São Paulo State University (UNESP), School of special oxidizable chlorophyl pigment in the reaction center, since Agricultural and Veterinary Sciences, Jaboticabal, state of São Paulo, most antenna (pigment-protein) complexes contain carotenoids that Brazil, under ambient conditions of light, relative humidity, and tem- confer photo-protection to the reaction center (Blankenship 2014). perature. The climatic conditions recorded during the experimental Among osmolytes acting in plant responses to environmental period (March 2014) were: mean temperature of 24.1°C, mean relative stresses, the quaternary ammonium glycine betaine has been ex- humidity of 76.8%, and mean day length of 12 h 08 min (Unesp 2020). tensively studied (Iqbal et al. 2005, Chen and Murata 2008, Ashraf Insects used in this research were reared according to method- 2009, Ali and Ashraf 2011), and its accumulation in maize depends ology adapted from Ávila et al. (2000). The colony of D. speciosa on plant variety (Quan et al. 2004). Glycine betaine is abundant was initiated from adults collected in common bean, Phaseolus vul- primarily in the chloroplast where it plays a vital role in protecting garis L. (Fabales: Fabaceae) (and surrounding weeds) grown in the the thylakoid membrane, contributing to maintenance of photosyn- experimental farm of UNESP, and wild insects were introduced every thetic efficiency (Genard et al. 1991) and allowing the plant to tol- two months to maintain genetic variability. erate different environmental stresses, mainly those of abiotic origin Maize seeds of cultivar ‘Cativerde 02’ were sown in 770-ml (Huang et al. 2000). Glycine betaine does not actively participate in plastic pots with an opening of 1.0 × 0.1 cm at
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