Evangelia Katsavou, Chara Sarafoglou, Vasileia Balabanidou, Evangelia Skoufa, Ralf Nauen, Marc Linka, Sven Geibel, Shane Denecke, John Vontas
{"title":"Characterisation of lepidopteran geranylgeranyl diphosphate synthase as a putative pesticide target","authors":"Evangelia Katsavou, Chara Sarafoglou, Vasileia Balabanidou, Evangelia Skoufa, Ralf Nauen, Marc Linka, Sven Geibel, Shane Denecke, John Vontas","doi":"10.1111/imb.12885","DOIUrl":"10.1111/imb.12885","url":null,"abstract":"<p>Geranylgeranyl pyrophosphate (diphosphate) synthase (GGPPS) plays an important role in various physiological processes in insects, such as isoprenoid biosynthesis and protein prenylation. Here, we functionally characterised the GGPPS from the major agricultural lepidopteran pests <i>Spodoptera frugiperda</i> and <i>Helicoverpa armigera</i>. Partial disruption of <i>GGPPS</i> by CRISPR in <i>S. frugiperda</i> decreased embryo hatching rate and larval survival, suggesting that this gene is essential. Functional expression <i>in vitro</i> of <i>Helicoverpa armigera</i> GGPPS in <i>Escherichia coli</i> revealed a catalytically active enzyme. Next, we developed and optimised an enzyme assay to screen for potential inhibitors, such as the zoledronate and the minodronate, which showed a dose-dependent inhibition. Phylogenetic analysis of GGPPS across insects showed that <i>GGPPS</i> is highly conserved but also revealed several residues likely to be involved in substrate binding, which were substantially different in bee pollinator and human GGPPS. Considering the essentiality of GGPPS and its putative binding residue variability qualifies a GGPPS as a novel pesticide target. The developed assay may contribute to the identification of novel insecticide leads.</p>","PeriodicalId":13526,"journal":{"name":"Insect Molecular Biology","volume":"33 2","pages":"147-156"},"PeriodicalIF":2.6,"publicationDate":"2023-11-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"92153698","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Juvenile hormone inhibits adult cuticle formation in Drosophila melanogaster through Kr-h1/Dnmt2-mediated DNA methylation of Acp65A promoter","authors":"Qianyu He, Xiaochun Fan, Shunxin Wang, Shanshan Chen, Jinxia Chen","doi":"10.1111/imb.12884","DOIUrl":"10.1111/imb.12884","url":null,"abstract":"<p>Differentiation of imaginal epidermal cells of <i>Drosophila melanogaster</i> to form adult cuticles occurs at approximately 40–93 h after puparium formation. Juvenile hormone (JH) given at pupariation results in formation of a second pupal cuticle in the abdomen instead of the adult cuticle. Although the adult cuticle gene <i>Acp65A</i> has been reported to be down-regulated following JH treatment, the regulatory mechanism remains unclear. Here, we found that the JH primary response gene <i>Krüppel homologue 1</i> (<i>Kr-h1</i>) plays a vital role in the repression of adult cuticle formation through the mediation of JH action. Overexpression of <i>Kr-h1</i> mimicked—while knocking down of <i>Kr-h1</i> attenuated—the inhibitory action of JH on the formation of the adult abdominal cuticle. Further, we found that Kr-h1 inhibited the transcription of <i>Acp65A</i> by directly binding to the consensus Kr-h1 binding site (KBS) within the <i>Acp65A</i> promoter region. Moreover, the DNA methyltransferase Dnmt2 was shown to interact with Kr-h1, combined with the KBS to promote the DNA methylation of sequences around the KBS, in turn inhibiting the transcription of <i>Acp65A</i>. This study advances our understanding of the molecular basis of the “status quo” action of JH on the <i>Drosophila</i> adult metamorphosis.</p>","PeriodicalId":13526,"journal":{"name":"Insect Molecular Biology","volume":"33 2","pages":"124-135"},"PeriodicalIF":2.6,"publicationDate":"2023-11-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"71423324","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
QiQige Wuyun, Yan Zhang, Jinxi Yuan, Jie Zhang, Cong Ren, Qi Wang, Shanchun Yan, Wei Liu, Guirong Wang
{"title":"A classic screening marker does not affect antennal electrophysiology but strongly regulates reproductive behaviours in Bactrocera dorsalis","authors":"QiQige Wuyun, Yan Zhang, Jinxi Yuan, Jie Zhang, Cong Ren, Qi Wang, Shanchun Yan, Wei Liu, Guirong Wang","doi":"10.1111/imb.12883","DOIUrl":"10.1111/imb.12883","url":null,"abstract":"<p>The key phenotype white eye (white) has been used for decades to selectively remove females before release in sterile insect technique programs and as an effective screening marker in genetic engineering. <i>Bactrocera dorsalis</i> is a representative tephritid pest causing damage to more than 150 fruit crops. Yet, the function of white in important biological processes remains unclear in <i>B. dorsalis</i>. In this study, the impacts of the <i>white</i> gene on electrophysiology and reproductive behaviour in <i>B. dorsalis</i> were tested. The results indicated that knocking out <i>Bdwhite</i> disrupted eye pigmentation in adults, consistent with previous reports. <i>Bdwhite</i> did not affect the antennal electrophysiology response to 63 chemical components with various structures. However, reproductive behaviours in both males and females were significantly reduced in <i>Bdwhite</i><sup>−/−</sup>. Both pre-copulatory and copulation behaviours were significantly reduced in <i>Bdwhite</i><sup>−/−</sup>, and the effect was male-specific. Mutant females significantly delayed their oviposition towards γ-octalactone, and the peak of oviposition behaviour towards orange juice was lost. These results show that <i>Bdwhite</i> might not be an ideal screening marker in functional gene research aiming to identify molecular targets for behaviour-modifying chemicals. Instead, owing to its strong effect on <i>B. dorsalis</i> sexual behaviours, the downstream genes regulated by <i>Bdwhite</i> or the genes from white-linked areas could be alternate molecular targets that promote the development of better behavioural modifying chemical-based pest management techniques.</p>","PeriodicalId":13526,"journal":{"name":"Insect Molecular Biology","volume":"33 2","pages":"136-146"},"PeriodicalIF":2.6,"publicationDate":"2023-10-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"50157802","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Transcriptome analysis of Apis mellifera antennae reveals molecular divergence underlying the division of labour in worker bees","authors":"Bairu Liu, Yicong Xu, Weixing Zhang","doi":"10.1111/imb.12882","DOIUrl":"10.1111/imb.12882","url":null,"abstract":"<p>The olfactory system plays a fundamental role in mediating insect behaviour. Worker bees exhibit an age-dependent division of labour, performing discrete sets of behaviours throughout their lifespan. The behavioural states of bees rely on their sense of the environment and chemical communication via their olfactory system, the antennae. However, the olfactory adaptation mechanism of worker bees during their behavioural development remains unclear. In this study, we conducted a comprehensive and quantitative analysis of antennal gene expression in the <i>Apis mellifera</i> of newly emerged workers, nurses, foragers and defenders using RNA-seq. We found that the antenna tissues of honey bees continued developing after transformation from newly emerged workers to adults. Additionally, we identified differentially expressed genes associated with bee development and division of labour. We validated that major royal jelly protein genes are highly and specifically expressed in nurse honey bee workers. Furthermore, we identified and validated significant alternative splicing events correlated with the development and division of labour. These findings provide a comprehensive transcriptome profile and a new perspective on the molecular mechanisms that may underlie the worker honey bee division of labour.</p>","PeriodicalId":13526,"journal":{"name":"Insect Molecular Biology","volume":"33 2","pages":"101-111"},"PeriodicalIF":2.6,"publicationDate":"2023-10-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"49677112","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Opsin diversity and evolution in the Elateroidea superfamily: Insights from transcriptome data","authors":"Danilo T. Amaral, Isabel A. S. Bonatelli","doi":"10.1111/imb.12881","DOIUrl":"10.1111/imb.12881","url":null,"abstract":"<p>Vision plays a vital biological role in organisms, which depends on the visual pigment molecules (opsin plus chromophore). The expansion or reduction of spectral channels in the organisms is determined by distinct opsin classes and copy numbers resulting from duplication or loss. Within Coleoptera, the superfamily Elateroidea exhibits a great diversity of morphological and physiological characteristics, such as bioluminescence, making this group an important model for opsin studies. While molecular and physiological studies have been conducted in Lampyridae and Elateridae, other families remain unexplored. Here, we reused transcriptome datasets from Elateroidea species, including members of Elateridae, Lampyridae, Phengodidae, Rhagophthalmidae, Cantharidae, and Lycidae, to detect the diversity of putative opsin genes in this superfamily. In addition, we tested the signature of sites under positive selection in both ultraviolet (UV)- and long-wavelength (LW)-opsin classes. Although the visual system in Elateroidea is considered simple, we observed events of duplication in LW- and UV-opsin, as well as the absence of UV-opsin in distinct families, such as larval Phengodidae individuals. We detected different copies of LW-opsins that were highly expressed in the eyes of distinct tribes of fireflies, indicating the possible selection of each copy during the evolution of the sexual mating to avoid spectrum overlapping. In Elateridae, we found that the bioluminescent species had a distinct LW-opsin copy compared with the non-bioluminescent species, suggesting events of duplication and loss. The signature of positive selection showed only one residue associated with the chromophore binding site in the Elateroidea, which may produce a bathochromic shift in the wavelength absorption spectra in this family. Overall, this study brings important content and fills gaps regarding opsin evolution in Elateroidea.</p>","PeriodicalId":13526,"journal":{"name":"Insect Molecular Biology","volume":"33 2","pages":"112-123"},"PeriodicalIF":2.6,"publicationDate":"2023-10-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41199713","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Amarish K. Yadav, Ramasamy Asokan, Akihiko Yamamoto, Anandrao A. Patil, Maxwell J. Scott
{"title":"Expansion of the genetic toolbox for manipulation of the global crop pest Drosophila suzukii: Isolation and assessment of eye colour mutant strains","authors":"Amarish K. Yadav, Ramasamy Asokan, Akihiko Yamamoto, Anandrao A. Patil, Maxwell J. Scott","doi":"10.1111/imb.12879","DOIUrl":"10.1111/imb.12879","url":null,"abstract":"<p><i>Drosophila suzukii</i> (Matsumura) (Diptera: Drosophilidae), commonly called spotted wing Drosophila, is an important agricultural pest recognised worldwide. <i>D. suzukii</i> is a pest of soft-skinned fruits as females can lay eggs in ripening fruit before harvest. While strains for genetic biocontrol of <i>D. suzukii</i> have been made, the development of transgenic <i>D. suzukii</i> strains and their further screening remain a challenge partly due to the lack of phenotypically trackable genetic-markers, such as those widely used with the model genetic organism <i>D. melanogaster</i>. Here, we have used CRISPR/Cas9 to introduce heritable mutations in the eye colour genes <i>white</i>, <i>cinnabar</i> and <i>sepia</i>, which are located on the X, second and third chromosomes, respectively. Strains were obtained, which were homozygous for a single mutation. Genotyping of the established strains showed insertion and/or deletions (indels) at the targeted sites. A strain homozygous for mutations in <i>cinnabar</i> and <i>sepia</i> showed a pale-yellow eye colour at eclosion but darkened to a sepia colour after a week. The fecundity and fertility of some of the <i>cinnabar</i> and <i>sepia</i> strains were comparable with the wild type. Although <i>white</i> mutant males were previously reported to be sterile, we found that sterility is not fully penetrant and we have been able to maintain white-eyed strains for over a year. The <i>cinnabar</i>, <i>sepia</i> and <i>white</i> mutant strains developed in this study should facilitate future genetic studies in <i>D. suzukii</i> and the development of strains for genetic control of this pest.</p>","PeriodicalId":13526,"journal":{"name":"Insect Molecular Biology","volume":"33 2","pages":"91-100"},"PeriodicalIF":2.6,"publicationDate":"2023-10-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/imb.12879","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41199712","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Wei-Kang Han, Feng-Xian Tang, Yang-Yang Yan, Yan Wang, Yi-Xi Zhang, Na Yu, Kan Wang, Ze-Wen Liu
{"title":"An OBP gene highly expressed in non-chemosensory tissues affects the phototaxis and reproduction of Spodoptera frugiperda","authors":"Wei-Kang Han, Feng-Xian Tang, Yang-Yang Yan, Yan Wang, Yi-Xi Zhang, Na Yu, Kan Wang, Ze-Wen Liu","doi":"10.1111/imb.12880","DOIUrl":"10.1111/imb.12880","url":null,"abstract":"<p>Insect odorant binding proteins (OBPs) were initially regarded as carriers of the odorants involved in chemosensation. However, it had been observed that a growing number of OBP genes exhibited broad expression patterns beyond chemosensory tissues. Here, an OBP gene (<i>OBP31</i>) was found to be highly expressed in the larval ventral nerve cord, adult brain and male reproductive organ of <i>Spodoptera frugiperda</i>. An <i>OBP31</i> knockout strain (<i>OBP31</i><sup><i>−/−</i></sup>) was generated by CRISPR/Cas9 mutagenesis. For <i>OBP31</i><sup><i>−/−</i></sup>, the larvae needed longer time to pupate, but there was no difference in the pupal weight between <i>OBP31</i><sup><i>−/−</i></sup> and wild type (WT). <i>OBP31</i><sup><i>−/−</i></sup> larvae showed stronger phototaxis than the WT larvae, indicating the importance of <i>OBP31</i> in light perception. For mating rhythm of adults, <i>OBP31</i><sup><i>−/−</i></sup> moths displayed an earlier second mating peak. In the cross-pairing of <i>OBP31</i><sup><i>−/−</i></sup> and WT moths, the mating duration was longer, and hatchability was lower in <i>OBP31</i><sup><i>−/−</i></sup> group and <i>OBP31</i><sup><i>+/−</i></sup>♂ group than that in the WT group. These results suggested that <i>OBP31</i> played a vital role in larval light perception and male reproductive process and could provide valuable insights into understanding the biological functions of OBPs that were not specific in chemosensory tissues.</p>","PeriodicalId":13526,"journal":{"name":"Insect Molecular Biology","volume":"33 1","pages":"81-90"},"PeriodicalIF":2.6,"publicationDate":"2023-10-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41182492","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Distinct roles of the Hox genes Ultrabithorax and abdominal-A in scorpionfly embryonic proleg development","authors":"Bing-Peng Liu, Bao-Zhen Hua","doi":"10.1111/imb.12878","DOIUrl":"10.1111/imb.12878","url":null,"abstract":"<p>The abdominal appendages of larval insects have a complex evolutionary history of gain and loss, but the regulatory mechanisms underlying the abdominal appendage development remain largely unclear. Here, we investigated the embryogenesis of abdominal prolegs in the scorpionfly <i>Panorpa liui</i> Hua (Mecoptera: Panorpidae) using in situ hybridization and parental RNA interference. The results show that RNAi-mediated knockdown of <i>Ultrabithorax</i> (<i>Ubx</i>) led to a homeotic transformation of the first abdominal segment (A1) into the third thoracic segment (T3) and changed the distributions of the downstream target <i>Distal-less</i> (<i>Dll</i>) expression but did not affect the expression levels of <i>Dll</i>. Knockdown of <i>abdominal-A</i> (<i>abd-A</i>) resulted in malformed segments, abnormal prolegs and disrupted <i>Dll</i> expression. The results demonstrate that the gene <i>Ubx</i> maintains an ancestral role of modulating A1 appendage fate without preventing <i>Dll</i> initiation, and a secondary adaptation of <i>abd-A</i> evolves the ability to specify abdominal segments and proleg identity. We conclude that changes in abdominal Hox gene expression and their target genes regulate abdominal appendage morphology during the evolutionary course of holometabolous larvae.</p>","PeriodicalId":13526,"journal":{"name":"Insect Molecular Biology","volume":"33 1","pages":"69-80"},"PeriodicalIF":2.6,"publicationDate":"2023-10-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41140579","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"The influence of first desaturase subfamily genes on fatty acid synthesis, desiccation tolerance and inter-caste nutrient transfer in the termite Coptotermes formosanus","authors":"Danni Xu, Yuxin Tong, Bosheng Chen, Baoling Li, Shengyin Wang, Dayu Zhang","doi":"10.1111/imb.12877","DOIUrl":"10.1111/imb.12877","url":null,"abstract":"<p>Desaturase enzymes play an essential role in the biosynthesis of unsaturated fatty acids (UFAs). In this study, we identified seven “first desaturase” subfamily genes (<i>Cfor-desatA1</i>, <i>Cfor-desatA2-a</i>, <i>Cfor-desatA2-b</i>, <i>Cfor-desatB-a</i>, <i>Cfor-desatB-b</i>, <i>Cfor-desatD</i> and <i>Cfor-desatE</i>) from the Formosan subterranean termite <i>Coptotermes formosanus</i>. These desaturases were highly expressed in the cuticle and fat body of <i>C. formosanus</i>. Inhibition of either the <i>Cfor-desatA2-a</i> or <i>Cfor-desatA2-b</i> gene resulted in a significant decrease in the contents of fatty acids (C16:0, C18:0, C18:1 and C18:2) in worker castes. Moreover, we observed that inhibition of most of desaturase genes identified in this study had a negative impact on the survival rate and desiccation tolerance of workers. Interestingly, when normal soldiers were reared together with <i>dsCfor-desatA2-b</i>-treated workers, they exhibited higher mortality, suggesting that desaturase had an impact on trophallaxis among <i>C. formosanus</i> castes. Our findings shed light on the novel roles of desaturase family genes in the eusocial termite <i>C. formosanus</i>.</p>","PeriodicalId":13526,"journal":{"name":"Insect Molecular Biology","volume":"33 1","pages":"55-68"},"PeriodicalIF":2.6,"publicationDate":"2023-09-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41121182","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"The silk gland proteome of Stenopsyche angustata provides insights into the underwater silk secretion","authors":"Yu-Jun Wang, Qing-Song Liu, Li-Ping Liu, Yi-Chuan Zhang, Shuang Qiu, Wen-Guang Zhang, Jin-Hang Lin, Yu-Ting Qin, Xin Wang, Yue-Ying Wu, Ping Zhao, Qing-You Xia, Ling Ding, Dong-Ying Rong, Hong Wang, Zhao-Ming Dong","doi":"10.1111/imb.12874","DOIUrl":"10.1111/imb.12874","url":null,"abstract":"<p>Caddisworms (Trichoptera) spin adhesive silks to construct a variety of underwater composite structures. Many studies have focused on the fibroin heavy chain of caddisworm silk and found that it contains heavy phosphorylation to maintain a stable secondary structure. Besides fibroins, recent studies have also identified some new silk proteins within caddisworm silk. To better understand the silk composition and its secretion process, this study reports the silk gland proteome of a retreat-building caddisworm, <i>Stenopsyche angustata</i> Martynov (Trichoptera, Stenopsychidae). Using liquid chromatography tandem mass spectrometry (LC-MS/MS), 2389 proteins were identified in the silk gland of <i>S. angustata</i>, among which 192 were predicted as secreted silk proteins. Twenty-nine proteins were found to be enriched in the front silk gland, whereas 109 proteins were enriched in the caudal silk gland. The fibroin heavy chain and nine uncharacterized silk proteins were identified as phosphorylated proteins. By analysing the sequence of the fibroin heavy chain, we found that it contains 13 Gly/Thr/Pro-rich regions, 12 Val/Ser/Arg-rich regions and a Gly/Arg/Thr-rich region. Three uncharacterized proteins were identified as sericin-like proteins due to their larger molecular weights, signal peptides and repetitive motifs rich in serine. This study provides valuable information for further clarifying the secretion and adhesion of underwater caddisworm silk.</p>","PeriodicalId":13526,"journal":{"name":"Insect Molecular Biology","volume":"33 1","pages":"41-54"},"PeriodicalIF":2.6,"publicationDate":"2023-09-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41127049","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}