- Comparative transcriptome analysis of the rice leaf folder ( Cnaphalocrocis medinalis ) to heat acclimation. - To understand the underlying mechanisms, we established a heat-acclimated strain via multigenerational selection at 39 °C. - After heat shock at 41 °C for 1 h, the transcriptomes of the heat-acclimated (S-39) and unacclimated (S-27) larvae were sequenced, using the unacclimated larvae without exposure to 41 °C as the control.. - Exposure to 41 °C induced 1160 differentially expressed genes (DEGs) between the heat-acclimated and unacclimated larvae. - Both the heat- acclimated and unacclimated larvae responded to heat stress via upregulating genes related to sensory organ development and structural constituent of eye lens, whereas the unacclimated larvae also upregulated genes related to structural constituent of cuticle. - Compared to unacclimated larvae, heat-acclimated larvae downregulated oxidoreductase activity-related genes when encountering heat shock. - Additionally, the unacclimated larvae also adjusted the spliceosome pathway, whereas the heat-acclimated larvae adjusted the biosynthesis of unsaturated fatty acids pathway when encountering heat stress. - Although the heat-acclimated and unacclimated larvae upregulated expression of heat shock protein genes under heat stress including HSP70, HSP27 and CRYAB, their biosynthesis, metabolism and detoxification-related genes expressed differentially.. - The heat-acclimated larvae induced more DEGs to response to heat shock than the unacclimated larvae. - The DEGs between heat-acclimated and unacclimated larvae after heat shock were enriched in the biosynthesis and metabolism pathways. - The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. - If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. - Approximately 58% of the odorant binding proteins obps genes in the antenna of Drosophila exhibit a change in expression after heat treatment [24]. - Eggs of the rice leaf folder can not hatch at 37 °C [31]. - More- over, high temperature affects host preference and shelter-building behaviour of the rice leaf folder larvae . - A previous study illustrated that the rice leaf folder larvae could increase their heat tolerance via heat selection, and heat shock protein genes were up- regulated in the selected larvae [36]. - Therefore, in this study, we successively selected the 3rd instar larvae at 39 °C for several genera- tions, and a heat-acclimated strain was generated which showed the similar survival rate under the 39 °C treat- ment as the control at 27 °C. - Then, we sequenced and analyzed the transcriptome of the 3rd instar larvae col- lected from the heat-acclimated strain (S-39) and the unacclimated strain (S-27) after exposure to 41 °C for 1 h, and the larvae from the unacclimated strain main- tained at 27 °C was the control (CK). - The differentially expressed genes (DEGs) in the S-39 vs CK, S-27 vs CK, and S-39 vs S-27, and GO and KEGG enrichment ana- lyses were performed. - The object of this experiment was to address the genes and pathways involving in the heat response and acclimation of the rice leaf folder larvae, which would highlight the molecular mechanism under- lying heat acclimation.. - The result showed that the rice leaf folder larvae could acclimate to heat stress at 39 °C via multigenerational heat selection (Fig. - After the raw reads were filtered, there were and clean reads obtained in the CK, S-27, and S-39, respectively.. - Differentially expressed genes between heat-acclimated and unacclimated larvae after heat exposure. - There were and 1160 differentially expressed genes (DEGs) distributed in the comparison of S-27 vs CK (Fig. - The heat-acclimated larvae (S-39) induced more DEGs to response to the heat exposure to 41 °C than the unacclimated larvae. - 2d), The heat-acclimated larvae shared 145 DEGs with the unac- climated larvae after exposure to 41 °C, but they uniquely expressed 1723 DEGs other than the unaccli- mated larvae (Fig. - selection/acclimation induced significant differentiation in gene expression of the rice leaf folder larvae when lar- vae were exposed to high temperature.. - When the heat- acclimated larvae were exposed to 41 °C, they induced 1868 DEGs, and these DEGs were significantly enriched in two GO terms: sensory organ development and struc- tural constituent of eye lens (Fig. - The expression of genes related to oxidoreductase activity was significantly downregulated in the S-39, compared to the S-27, but it was not different between the S-27 and CK (Fig. - KEGG pathway enrichment analysis showed that DEGs induced by the heat exposure to 41 °C in both the heat-acclimated and unacclimated larvae were signifi- cantly enriched in the same pathways: longevity regulat- ing, protein processing in endoplasmic reticulum, antigen processing and presentation, MAPK signaling, legionellosis, toxoplasmosis,estrogen signaling, and endocytosis, suggesting the general immune or cellular responses to heat stress (Table 1). - In the unacclimated larvae, there were eight DEGs enriched in the pathway. - of spliceosome, whereas in the heat-acclimated larvae there were eight DEGs enriched in the pathway of bio- synthesis of unsaturated fatty acids (Table 1). - The DEGs between heat-acclimated and unacclimated larvae after heat treatment were signficiantly enriched in metabolism pathways, such as the retinol, porphyrin and chlorophyll, ascorbate and aldarate, and drug metabolism (Table 1).. - Besides these up- regulated heat shock protein genes, the heat-acclimated larvae also upregulated other 25 genes and downregu- lated nine genes including the heat shock protein gene HSP90A in response to the heat stress (Table 1).. - The differentially expressed genes between S-27 and S-39 were significantly enriched in eight pathways, seven in which were involved in metabolism and one involved in the steroid hormone biosynthesis. - After expsoure to 41 °C for 1 h, the heat- acclimated larvae downregulated SDR16C5, RDH12, hemH, GNL, UPB1, DPYD and EPHX1 genes and upreg- ulated GST gene, compared to the unacclimated larvae (Table 1).. - Expression levels of oxidoreductase activity-related genes in the heat-acclimated and unacclimated larvae after heat shock. - The expression levels of the oxidoreductase activity- related gene, glucose dehydrogenase (GLD-71513) were. - Cluster of nine larvae samples and 21 DEGs enriched in the GO term of oxidoreductase activity based on their expression levels (d). - significantly affected by the heat acclimation (F P <. - 0.001) and the heat exposure duration to 41 °C (F P = 0.001, Fig. - The relative expression levels of oxidoreductase activity-related genes were lower in the heat-acclimated larvae than that in the unacclimated larvae (Fig. - Moreover, in this study, we found that the rice leaf folder larvae also changed gene expression to respond to heat stress and heat acclimation/adaptation. - Under heat stress, the differentially expressed genes of the heat- acclimated and unacclimated larvae were significantly Table 1 KEGG pathway enrichment for the DEGs between S-27, S-39, and CK. - The heat-acclimated larvae triggered more genes to respond to heat stress than the unacclimated larvae via changes in gene expression. - In the silkworm larvae, the thermotolerant strain induced more DEGs to en- counter high temperature than the thermosensitive strain [39]. - Insects regulate gene expression levels to re- spond to heat shock, and the heat acclimated or condi- tioned larvae trigger more genes involving in this response.. - In this study, we found that both the heat-acclimated and unacclimated larvae increaesd the expression levels of HSP27, CRYAB and HSP70, when encountering the heat exposure to 41 °C, but addintion- ally, the heat-acclimated larvae decreased the expression of the HSP90A. - The global transcriptome results indi- cated that HSP genes might have different expession pat- terns in the heat-acclimated and unacclimated larvae.. - HSP70, HSP27, and CRYAB genes were upregulated in both the heat-acclimated and unacclimated larvae ex- posed to high temperature, suggesting that these genes might be involved in the rapid response to heat stress, but the HSP90A was downregulated or did not change in the heat-acclimated larvae when exposed to heat, which might be involved in the slowly developing heat acclimation or adaptation. - The RT-qPCR detection also supported this expression mode of HSP70 and HSP90 in the rice leaf folder larvae [36]. - Heat shock protein gene family are involved in the response and acclimation to heat stress.. - In the present study, when lar- vae were exposed to 41 °C for 1 h, the significantly enriched GO terms for DEGs in the unacclimated larvae. - were involved in the sensory organ development, struc- tural consitituent of eye lens, and structural consitituent of cuticle, but the enriched GO terms in the heat- acclimated larvae were involved in the sensory organ de- velopment and structural consitutent of eye lens, but not the cuticle. - After multigenerational heat acclima- tion, the sensitivity of cuticle to heat may become lower than before, and therefore, the heat-induced DEGs are not enriched in the GO term of structural consitituent of cuticle anymore. - Cuticle protein genes are involved in the cuticle formation, and they are necessary for cuticle development, flexibility, and metamorphosis [45]. - Transcrip- tional patterns of genes encoding cuticle proteins in the water flea Daphnia pulex have responses to the inter- action between biotic (predator presence) and abiotic (low calcium concentration) environmental stresses [47].. - In this study, we found that cuticle protein genes in the rice leaf folder larvae were expressed differentially induced by heat exposure. - Cuticle protein genes may be involved in the response of this insect to heat stress. - We found that both the heat-acclimated and unaccli- mated larvae were significantly enriched for DEGs in similar KEGG pathways related to longevity regulating,. - These path- ways might be involved in the response of the rice leaf folder larvae to heat stress. - In this study, furthermore, we found that the differ- ent KEGG pathways enriched for DEGs in the heat- acclimated and unacclimated larvae when they were ex- posed to heat stress. - For example, the pathway of spli- ceosome was enriched for DEGs in the unacclimated larvae, showing that DHX38 and UAP56 genes were up- regulated and SYF1 gene dowregulated, but not enriched in the heat-acclimated larvae. - On the contrary, pathway of the biosynthesis of unsaturated fatty acids was signifi- cantly enriched for DEGs in the heat-acclimated larvae, but not in the unacclimated larvae. - The DEGs between the heat-acclimated and unaccli- mated larvae were mainly enriched in the GO term of the molecular function on oxidoreductase activity when larvae were treated by high temperature. - These results show that oxidoreductases play important roles in the developmental or physiological process, such as ecdysteroid and glucose metabolism. - RNA inference of ecdysone oxidase results in the accumulation of ecdysteroid and death of larvae or pupae of silkworms [49]. - The metabolic path- ways play a significantly role in the high temperature tol- erance of silkworms [39, 51]. - In the rice leaf folder, we found that the significant differently expressed genes be- tween heat-acclimated and unacclimated larvae were mainly involved in metabolism of retinol, porphyurin and chlorophyll, ascorbate and aldarate, and drug. - Genes UGT, RDH, SDR and GST were expressed differentially between heat-acclimated and unacclimated larvae in re- sponse to heat stress. - We found that after treatment at 41 °C for 1 h, expression of GSTs was significantly up-regulated in the heat-acclimated larvae, compared to the unacclimated larvae. - These genes related to sensory organ development and structural constituent of eye lens and cuticle are in- volved in the response. - The oxidoreductase activity- related genes are down-regulated to alleviate the heat in- juries. - The larvae of rice leaf folder acclimated to heat stress via multigenerational selection. - The heat-acclimated lar- vae regulated expression of more genes to response to heat shock than the unacclimated larvae. - Genes related to sensory organ development and structural constituent might modulate the rapid response of larvae to heat stress, and genes involved in the oxidoreductase activity might be associated with heat acclimation. - The temperature in the chamber increased or decreased by 3 °C in 8 min. - After 3 h, the temperature was set at and 27 °C at and 15:30 (local time), respectively, and maintained at 27 °C until the heat treatment was performed again in the next day.. - The differ- ences in survival rates between the heat selected and unselected larvae were analysed using the Mann- Whitney U test, because the data in the sixth generation of heat selection did not meet the normal distribution.. - 1), and therefore, we considered the heat treated popula- tion as a heat-acclimated strain and the population reared at 27 °C as an unacclimated strain.. - Heat exposure on the heat-acclimated and unacclimated strains. - When the heat-acclimated strain was selected for 15 genera- tions at 39 °C, 30 third-instar larvae were collected and trans- ferred onto wheat seedlings. - Thirty larvae from the unacclimated strain were also performed this heat treatment as the heat-acclimated larvae. - These larval samples exposed to 41 °C were named S-39 and S-27 for the heat-acclimated and unacclimated larvae, respectively.. - The red parts mean items only belonging to the heat-acclimated larvae, the blue parts belonging to the unacclomated larvae, and black parts belonging to both the heat-acclimated and unacclimated larvae. - The 3rd-instar larvae collected from the heat-acclimated (S-39) and unacclimated (S-27) strains were exposed to 41 °C for and 3 h. - Sequences of the two putative glucose dehydrogenase genes (GLD) in the transcriptome. - The funding body has no role in the design of the study and collection, analysis, and interpretation of data and in writing the manuscript.. - Impact of different temperatures on survival and energy metabolism in the Asian citrus psyllid, Diaphorina citri Kuwayama. - Host choice, settling and folding leaf behaviors of the larval rice leaf folder under heat stress. - Stress-induced thermotolerance of ventilatory motor pattern generation in the locust, Locusta migratoria. - Evaluating responses to temperature during pre-metamorphosis and carry- over effects at post-metamorphosis in the wood tiger moth (Arctia plantaginis). - Silkworm thermal biology: a review of heat shock response, heat shock proteins and heat acclimation in the domesticated silkworm, Bombyx mori. - Heat shock suppresses mating and sperm transfer in the rice leaf folder Cnaphalocrocis medinalis. - Can the young larvae of Cnaphalocrocis medinalis (Lepidoptera: Pyralidae) tolerate the heat stress in summer? Environ Entomol. - Behavioural adaptation of the rice leaf folder Cnaphalocrocis medinalis to short-term heat stress. - Multigenerational heat acclimation increases thermal tolerance and expression levels of Hsp70 and Hsp90 in the rice leaf folder larvae. - glycosyltransferases in the two Heliothine moth species Helicoverpa armigera and Heliothis virescens. - Interaction of ferulic acid with glutathione S-transferase and carboxylesterase genes in the brown planthopper, Nilaparvata lugens. - detoxification in the rice leaf fold (Cnaphalocrocis medinalis) larvae through transcriptomic analysis
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