Scientia Agricultura Sinica ›› 2023, Vol. 56 ›› Issue (1): 79-89.doi: 10.3864/j.issn.0578-1752.2023.01.006

• PLANT PROTECTION • Previous Articles     Next Articles

Cloning of Small Heat Shock Protein Gene Hsp21.9 in Sitodiplosis mosellana and Its Expression Characteristics During Diapause and Under Temperature Stresses

GU LiDan1(),LIU Yang1,LI FangXiang2,CHENG WeiNing1,*()   

  1. 1. College of Plant Protection, Northwest A&F University/Key Laboratory of Integrated Pest Management on Crops in Northwestern Loess Plateau, Ministry of Agriculture and Rural Affairs, Yangling 712100, Shaanxi
    2. Xi’an Agricultural Technology Extension Centre, Xi’an 710061
  • Received:2022-07-25 Accepted:2022-09-08 Online:2023-01-01 Published:2023-01-17
  • Contact: WeiNing CHENG E-mail:826185856@qq.com;cwning@126.com

RichHTML

44

PDF

131

Abstract:

【Objective】The wheat blossom midge Sitodiplosis mosellana (Diptera: Cecidomyiidae), one of the most important wheat pests, undergoes obligatory larval diapause to survive adverse temperature extremes during hot summers and cold winters. This study aims to explore the potential roles of small heat shock protein (sHsp) gene Hsp21.9 in diapause process of S. mosellana. 【Method】 RACE and RT-PCR technologies were used to clone the full-length cDNA of Hsp21.9 from S. mosellana pre-diapause larvae. Bioinformatics programs were used to characterize the nucleotide and amino acid sequence of cloned Hsp21.9. Real-time quantitative PCR (RT-qPCR) was used to determine the mRNA expression level of Hsp21.9 in pre-diapause, diapause, post-diapause quiescent and developing larvae of S. mosellana, as well as over-summering larvae exposed to short-term (≤120 min) heat stress (35-50℃) and over-wintering larvae exposed to short-term (≤120 min) cold stress (0 to -15℃). The recombinant Hsp21.9 protein was expressed by Escherichia coli prokaryotic expression technology, and then purified. The activity of bacterially expressed recombinant proteins to suppress thermal aggregation of pig heart mitochondrial malate dehydrogenase (MDH) was determined by colorimetry. 【Result】The full-length cDNA of S. mosellana Hsp21.9 (SmHsp21.9) obtained was 1 087 bp (GenBank accession number: KT749988), which contained a 582 bp open reading frame (ORF). The predicted ORF encoded a protein of 193 amino acids of which the content of glutamic acid (12.4%) was the most, and the content of cysteine (0.5%) was the least. The estimated molecular weight and isoelectric point were 21.9 kD and 5.67, respectively. The amino acid sequence of SmHsp21.9 contains typical α-crystallin domain of the sHsp family. The domain consists of six β-sheets, which forms a β-sandwich structure. Sequence alignment and phylogenetic analysis suggested that SmHsp21.9 displayed the highest amino acid identity and the closest relationship to Hsp27 from the Nematocera Chironomus riparius. RT-qPCR indicated that SmHsp21.9 expression differed significantly among different diapause stages. The expression level was decreased after the initiation of diapause, gradually increased in October, and peaked in early-to-mid phase of post-diapause (December and January). Compared with the untreated control, the expression level of SmHsp21.9 was significantly induced in over-summering larvae exposed to heat stress (35-45℃) or over-wintering larvae exposed to cold stressed (-5 to -10℃), but temperature extremes i.e. as high as 50℃ or as low as -15℃ failed to do so. The treatment duration also affected transcript levels of SmHsp21.9, with the maximum value at 30-60 min. Recombinant SmHsp21.9 proteins obtained significantly prevented heat-induced (43℃) aggregation of MDH, suggesting its significant molecular chaperone functionality. 【Conclusion】The expression of SmHsp21.9 is regulated not only by diapause development, but also by environmental temperature. SmHsp21.9 might be involved in initiation and termination of diapause, and heat/cold tolerance during diapause in S. mosellana.

Key words: Sitodiplosis mosellana, Hsp21.9, gene cloning, diapause, temperature stress, gene expression

Table 1

Primers used in this study"

引物Primer 序列Sequence (5′ to 3′) 用途Purpose
Hsp21.9-3′-outer TACCGTCGTTCCACTAGTGATTT 3′ RACE
Hsp21.9-3′-inner CGCGGATCCTCCACTAGTGATTTCACTATAGG
Hsp21.9-5′-outer CATGGCTACATGCTGACAGCCTA 5′ RACE
Hsp21.9-5′-inner CGCGGATCCACAGCCTACTGATGATCAGTCGATG
Hsp21.9-all-F GCTATTTACGAGCAATCAC cDNA全长验证
Full-length cDNA validation
Hsp21.9-all-R GCGCAATAATCTGCCAATA
Hsp21.9-q-F GATTCAAGCCAGAGCAAGT 实时定量PCR
Real-time quantitative PCR
Hsp21.9-q-R GGTTTCAGGTTTCGGACAT
GADPH-q-F CCATCAAAGCAAGCAAGA
GADPH-q-R CAGCACGGAGCACAAGAC
Hsp21.9-F GGAATTCAAATTAAAGTGTGAACAATGTCGCT (EcoR Ⅰ) 原核表达
Prokaryotic expression
Hsp21.9-R CCCAAGCTTCATTATTTCTTCTCATCTGTTTTCT (Hind Ⅲ)

Fig. 1

Nucleotide and deduced amino acid sequence of SmHsp21.9 Start codon (ATG) and stop codon (TAA) were boxed; the putative polyadenylation signal (AATAAA) was underlined; α-crystallin domain was shaded; IXI motif was indicated with oval"

Fig. 2

Predicted three-dimensional structure of SmHsp21.9 α-crystallin domain based on SWISS-MODEL server N and C denote the N- and C-terminal, respectively; the blue and green sheets are the β-sheet structures of two individual monomers; the arrows indicate the amino acid sequence from N-terminal to C-terminal; the red parts are α-helices"

Fig. 3

Phylogenetic relationship of SmHsp21.9 and sHsps from other insects"

Fig. 4

Relative expression level of SmHsp21.9 in pre-diapause, diapause and post-diapause larvae of S. mosellana The data in the figure are mean±SE, different lowercase letters above bars show significant difference at 0.05 level by Duncan’s multiple range test (P<0.05). The same as Fig. 5, Fig. 6"

Fig. 5

Relative expression level of SmHsp21.9 in over-summering larvae heat-stressed by different high temperatures for 1 h (A), and 40, 45℃ for different times (B)"

Fig. 6

Relative expression level of SmHsp21.9 in over-wintering larvae cold-stressed by different low temperatures for 1 h (A), and -5, -10℃ for different times (B)"

Fig. 7

SDS-PAGE analysis of recombinant SmHsp21.9 protein expression"

Fig. 8

Molecular chaperone activity of SmHsp21.9 demonstrated by the malate dehydrogenase (MDH) thermal aggregation assay"

[1] SHRESTHA G, REDDY G V P. Field efficacy of insect pathogen, botanical, and jasmonic acid for the management of wheat midge Sitodiplosis mosellana and the impact on adult parasitoid Macroglenes penetrans populations in spring wheat. Insect Science, 2019, 26(3): 523-535.
doi: 10.1111/1744-7917.12548
[2] WANG Q, LIU X B, LIU H, FU Y, CHENG Y M, ZHANG L J, SHI W P, ZHANG Y, CHEN J L. Transcriptomic and metabolomic analysis of wheat kernels in response to the feeding of orange wheat blossom midges (Sitodiplosis mosellana) in the field. Journal of Agricultural and Food Chemistry, 2022, 70(5): 1477-1493.
doi: 10.1021/acs.jafc.1c06239
[3] 王越, 龙治任, 冯安荣, 成卫宁. 虫口基数、小麦品种和降水对麦红吸浆虫危害程度的影响. 西北农业学报, 2015, 24(10): 165-171.
WANG Y, LONG Z R, FENG A R, CHENG W N. Effects of initial population number, wheat varieties and precipitation on infestation of Sitodiplosis mosellana (Diptera: Cecidomyiidae). Acta Agriculture Boreali-Occidentalis Sinica, 2015, 24(10): 165-171. (in Chinese)
[4] CHENG W N, LONG Z R, ZHANG Y D, LIANG T T, ZHU- SALZMAN K Y. Effects of temperature, soil moisture and photoperiod on diapause termination and post-diapause development of the wheat blossom midge, Sitodiplosis mosellana (Géhin)(Diptera: Cecidomyiidae). Journal of Insect Physiology, 2017, 103: 78-85.
doi: 10.1016/j.jinsphys.2017.10.001
[5] GU J, HUANG L X, SHEN Y, HUANG L H, FENG Q L. Hsp70 and small Hsps are the major heat shock protein members involved in midgut metamorphosis in the common cutworm, Spodoptera litura. Insect Molecular Biology, 2012, 21(5): 535-543.
doi: 10.1111/j.1365-2583.2012.01158.x pmid: 22957810
[6] SHEN Q D, ZHAO L N, XIE G Q, WEI P, YANG M M, WANG S G, ZHANG F, TANG B. Cloning three Harmonia axyridis (Coleoptera: Coccinellidae) heat shock protein 70 family genes: Regulatory function related to heat and starvation stress. Journal of Entomological Science, 2015, 50(3): 168-185.
doi: 10.18474/JES14-30.1
[7] FRANCK E, MADSEN O, VAN RHEEDE T, RICARD G, HUYNEN M A, DE JONG W W. Evolutionary diversity of vertebrate small heat shock proteins. Journal of Molecular Evolution, 2004, 59(6): 792-805.
pmid: 15599511
[8] KAPPÉ G, FRANCK E, VERSCHUURE P, BOELENS W C, LEUNISSEN J A, DE JONG W W. The human genome encodes 10 alpha-crystallin-related small heat shock proteins: HspB1-10. Cell Stress & Chaperones, 2003, 8(1): 53-61.
doi: 10.1379/1466-1268(2003)8<53:THGECS>2.0.CO;2
[9] LI Z, LI X, YU Q Y, XIANG Z H, KISHINO H, ZHANG Z. The small heat shock protein (sHSP) genes in the silkworm, Bombyx mori, and comparative analysis with other insect sHSP genes. BMC Evolutionary Biology, 2009, 9: 215.
doi: 10.1186/1471-2148-9-215
[10] 汪慧娟, 赵静, 施佐堃, 邱玲玉, 王甦, 张帆, 王世贵, 唐斌. 异色瓢虫3个小分子热激蛋白序列及低温诱导表达分析. 中国农业科学, 2017, 50(16): 3145-3154.
WANG H J, ZHAO J, SHI Z K, QIU L Y, WANG S, ZHANG F, WANG S G, TANG B. Sequence analysis and induced expression of three novel small heat shock proteins mediating cold-hardiness in Harmonia axyridis. Scientia Agricultura Sinica, 2017, 50(16): 3145-3154. (in Chinese)
[11] ZHANG Y Y, LIU Y L, GUO X L, LI Y L, GAO H R, GUO X Q, XU B H. sHsp22.6, an intronless small heat shock protein gene, is involved in stress defence and development in Apis cerana cerana. Insect Biochemistry and Molecular Biology, 2014, 53: 1-12.
doi: 10.1016/j.ibmb.2014.06.007
[12] ZAHUR M, MAQBOOL A, IRFAN M, BAROZAI M Y K, QAISER U, RASHID B, HUSNAIN T, RIAZUDDIN S. Functional analysis of cotton small heat shock protein promoter region in response to abiotic stresses in tobacco using Agrobacterium-mediated transient assay. Molecular Biology Reports, 2009, 36(7): 1915-1921.
doi: 10.1007/s11033-008-9399-9
[13] ZHANG A G, LU Y L, LI C H, ZHANG P, SU X R, LI Y, WANG C L, LI T W. A small heat shock protein (sHSP) from Sinonovacula constricta against heavy metals stresses. Fish & Shellfish Immunology, 2013, 34(6): 1605-1610.
[14] HUANG L H, WANG C Z, KANG L. Cloning and expression of five heat shock protein genes in relation to cold hardening and development in the leafminer, Liriomyza sativa. Journal of Insect Physiology, 2009, 55(3): 279-285.
doi: 10.1016/j.jinsphys.2008.12.004 pmid: 19133268
[15] XIE J, HU X X, ZHAI M F, YU X J, SONG X W, GAO S S, WU W, LI B. Characterization and functional analysis of hsp18.3 gene in the red flour beetle, Tribolium castaneum. Insect Science, 2019, 26(2): 263-273.
doi: 10.1111/1744-7917.12543
[16] RINEHART J P, LI A Q, YOCUM G D, ROBICH R M, HAYWARD S A L, DENLINGER D L. Up-regulation of heat shock proteins is essential for cold survival during insect diapause. Proceedings of the National Academy of Sciences of the United States of America, 2007, 104(27): 11130-11137.
[17] SI F L, HE Z B, CHEN B. Cloning and expression profiling of heat shock protein DaHSP23 gene in the winter and summer diapause pupae of the onion maggot, Delia antiqua (Diptera: Anthomyiidae). Acta Entomologica Sinica, 2016, 59(4): 402-410.
[18] LU Y X, XU W H. Proteomic and phosphoproteomic analysis at diapause initiation in the cotton bollworm, Helicoverpa armigera. Journal of Proteome Research, 2010, 9(10): 5053-5064.
doi: 10.1021/pr100356t
[19] ZHANG B, ZHENG J C, PENG Y, LIU X X, HOFFMANN A A, MA C S. Stress responses of small heat shock protein genes in lepidoptera point to limited conservation of function across phylogeny. PLoS ONE, 2015, 10(7): e0132700.
[20] TACHIBANA S I, NUMATA H, GOTO S G. Gene expression of heat-shock proteins (Hsp23, Hsp70 and Hsp90) during and after larval diapause in the blow fly Lucilia sericata. Journal of Insect Physiology, 2005, 51(6): 641-647.
doi: 10.1016/j.jinsphys.2004.11.012
[21] GOTO S G, KIMURA M T. Heat-shock-responsive genes are not involved in the adult diapause of Drosophila triauraria. Gene, 2004, 326(1): 117-122.
doi: 10.1016/j.gene.2003.10.017
[22] ZHAO J J, HUANG Q T, ZHANG G J, ZHU-SALZMAN K Y, CHENG W N. Characterization of two small heat shock protein genes (Hsp17.4 and Hs20.3) from Sitodiplosis mosellana, and their expression regulation during diapause. Insects, 2021, 12: 119.
doi: 10.3390/insects12020119
[23] CHENG W N, LI D, WANG Y, LIU Y, ZHU-SALZMAN K Y. Cloning of heat shock protein genes (hsp70, hsc70 and hsp90) and their expression in response to larval diapause and thermal stress in the wheat blossom midge, Sitodiplosis mosellana. Journal of Insect Physiology, 2016, 95: 66-77.
doi: 10.1016/j.jinsphys.2016.09.005
[24] DOANE J F, OLFERT O. Seasonal development of wheat midge, Sitodiplosis mosellana (Géhin) (Diptera: Cecidomyiidae), in Saskatchewan, Canada. Crop Protection, 2008, 27(6): 951-958.
doi: 10.1016/j.cropro.2007.11.016
[25] LIVAK K J, SCHMITTGEN T D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods, 2001, 25(4): 402-408.
doi: 10.1006/meth.2001.1262
[26] CHENG W N, ZHANG Y D, LIU W, LI G W, ZHU-SALZMAN K Y. Molecular and functional characterization of three odorant-binding proteins from the wheat blossom midge, Sitodiplosis mosellana. Insect Science, 2020, 27(4): 721-734.
doi: 10.1111/1744-7917.12677
[27] PÉREZ-MORALES D, OSTOA-SALOMA P, ESPINOZA B. Trypanosoma cruzi SHSP16: Characterization of an α-crystallin small heat shock protein. Experimental Parasitology, 2009, 123: 182-189.
doi: 10.1016/j.exppara.2009.06.019
[28] FU X, LI W, MAO Q, CHANG Z. Disulfide bonds convert small heat shock protein Hsp16.3 from a chaperone to a non-chaperone: Implications for the evolution of cysteine in molecular chaperones. Biochemical and Biophysical Research Communications, 2003, 308(3): 627-635.
pmid: 12914797
[29] JACOBSEN J V, SHAW D C. Heat-stable proteins and abscisic acid action in barley aleurone cells. Plant Physiology, 1989, 91(4): 1520-1526.
doi: 10.1104/pp.91.4.1520 pmid: 16667211
[30] BAGNERIS C, BATEMAN O A, NAYLOR C E, CRONIN N, BOELENS W C, KEEP N H, SLINGSBY C. Crystal structures of α-crystallin domain dimers of αB-crystallin and Hsp20. Journal of Molecular Biology, 2009, 392: 1242-1252.
doi: 10.1016/j.jmb.2009.07.069
[31] SUN Y, MACRAE T H. Small heat shock proteins: Molecular structure and chaperone function. Cellular and Molecular Life Sciences, 2005, 62(21): 2460-2476.
doi: 10.1007/s00018-005-5190-4 pmid: 16143830
[32] GKOUVITSAS T, KONTOGIANNATOS D, KOURTI A. Differential expression of two small Hsps during diapause in the corn stalk borer Sesamia nonagrioides (Lef.). Journal of Insect Physiology, 2008, 54(12): 1503-1510.
doi: 10.1016/j.jinsphys.2008.08.009
[33] KOKOLAKIS G, TATARI M, ZACHAROPOULOU A, MINTZAS A C. The hsp27 gene of the Mediterranean fruit fly, Ceratitis capitata: Structural characterization, regulation and developmental expression. Insect Molecular Biology, 2008, 17(6): 699-710.
doi: 10.1111/j.1365-2583.2008.00840.x
[34] LIU Z H, YAO P B, GUO X Q, XU B H. Two small heat shock protein genes in Apis cerana cerana: Characterization, regulation, and developmental expression. Gene, 2014, 545(2): 205-214.
doi: 10.1016/j.gene.2014.05.034
[35] SHEN Y, GU J, HUANG L H, ZHENG S C, LIU L, XU W H, FENG Q L, KANG L. Cloning and expression analysis of six small heat shock protein genes in the common cutworm, Spodoptera litura. Journal of Insect Physiology, 2011, 57(7): 908-914.
doi: 10.1016/j.jinsphys.2011.03.026 pmid: 21510953
[36] 成卫宁, 李建军, 李怡萍, 李修炼, 仵均祥, 王洪亮. 小麦吸浆虫成虫和幼虫滞育过程中蜕皮激素的定量分析. 植物保护学报, 2009, 36(2): 163-167.
CHENG W N, LI J J, LI Y P, LI X L, WU J X, WANG H L. Quantitative analysis of ecdysteroid in adults and the pre-diapause, diapause and post-diapause larvae of wheat blossom midge, Sitodiplosis mosellana Gehin. Acta Phytophylacica Sinica, 2009, 36(2): 163-167. (in Chinese)
[37] 史学凯, 寇利花, 张育平, 马恩波, 张建珍, 吴海花. 温度对中华稻蝗小分子热休克蛋白基因表达的影响. 应用昆虫学报, 2016, 53(6): 1267-1273.
SHI X K, KOU L H, ZHANG Y P, MA E B, ZHANG J Z, WU H H. Effects of temperature on the expression patterns of OcsHSP genes in Oxya chinensis. Chinese Journal of Applied Entomology, 2016, 53(6): 1267-1273. (in Chinese)
[38] GARCIA-REINA A, RODRIGUEZ-GARCIA M J, RAMIS G, GALIAN J. Real-time cell analysis and heat shock protein gene expression in the TcA Tribolium castaneum cell line in response to environmental stress conditions. Insect Science, 2017, 24(3): 358-370.
doi: 10.1111/1744-7917.12306
[39] 刘魏魏, 杨璞, 陈晓鸣. 白蜡虫热激蛋白基因在低温胁迫下的表达分析. 林业科学研究, 2013, 26(6): 681-685.
LIU W W, YANG P, CHEN X M. Expression analysis of heat shock protein genes in Ericerus pela under cold stress. Forest Research, 2013, 26(6): 681-685. (in Chinese)
[1] ZHANG KeKun,CHEN KeQin,LI WanPing,QIAO HaoRong,ZHANG JunXia,LIU FengZhi,FANG YuLin,WANG HaiBo. Effects of Irrigation Amount on Berry Development and Aroma Components Accumulation of Shine Muscat Grape in Root-Restricted Cultivation [J]. Scientia Agricultura Sinica, 2023, 56(1): 129-143.
[2] WANG JunJuan,LU XuKe,WANG YanQin,WANG Shuai,YIN ZuJun,FU XiaoQiong,WANG DeLong,CHEN XiuGui,GUO LiXue,CHEN Chao,ZHAO LanJie,HAN YingChun,SUN LiangQing,HAN MingGe,ZHANG YueXin,FAN YaPeng,YE WuWei. Characteristics and Cold Tolerance of Upland Cotton Genetic Standard Line TM-1 [J]. Scientia Agricultura Sinica, 2022, 55(8): 1503-1517.
[3] DONG SangJie,JIANG XiaoChun,WANG LingYu,LIN Rui,QI ZhenYu,YU JingQuan,ZHOU YanHong. Effects of Supplemental Far-Red Light on Growth and Abiotic Stress Tolerance of Pepper Seedlings [J]. Scientia Agricultura Sinica, 2022, 55(6): 1189-1198.
[4] LAI ChunWang, ZHOU XiaoJuan, CHEN Yan, LIU MengYu, XUE XiaoDong, XIAO XueChen, LIN WenZhong, LAI ZhongXiong, LIN YuLing. Identification of Ethylene Synthesis Pathway Genes in Longan and Its Response to ACC Treatment [J]. Scientia Agricultura Sinica, 2022, 55(3): 558-574.
[5] SHU JingTing,SHAN YanJu,JI GaiGe,ZHANG Ming,TU YunJie,LIU YiFan,JU XiaoJun,SHENG ZhongWei,TANG YanFei,LI Hua,ZOU JianMin. Relationship Between Expression Levels of Guangxi Partridge Chicken m6A Methyltransferase Genes, Myofiber Types and Myogenic Differentiation [J]. Scientia Agricultura Sinica, 2022, 55(3): 589-601.
[6] LI YuZe,ZHU JiaWei,LIN Wei,LAN MoYing,XIA LiMing,ZHANG YiLi,LUO Cong,HUANG Gui Xiang,HE XinHua. Cloning and Interaction Protein Screening of RHF2A Gene from Xiangshui Lemon [J]. Scientia Agricultura Sinica, 2022, 55(24): 4912-4926.
[7] GUO ShaoLei,XU JianLan,WANG XiaoJun,SU ZiWen,ZHANG BinBin,MA RuiJuan,YU MingLiang. Genome-Wide Identification and Expression Analysis of XTH Gene Family in Peach Fruit During Storage [J]. Scientia Agricultura Sinica, 2022, 55(23): 4702-4716.
[8] ZHANG Chuan,LIU Dong,WANG HongZhang,REN Hao,ZHAO Bin,ZHANG JiWang,REN BaiZhao,LIU CunHui,LIU Peng. Effects of High Temperature Stress in Different Periods on Dry Matter Production and Grain Yield of Summer Maize [J]. Scientia Agricultura Sinica, 2022, 55(19): 3710-3722.
[9] KANG Chen,ZHAO XueFang,LI YaDong,TIAN ZheJuan,WANG Peng,WU ZhiMing. Genome-Wide Identification and Analysis of CC-NBS-LRR Family in Response to Downy Mildew and Powdery Mildew in Cucumis sativus [J]. Scientia Agricultura Sinica, 2022, 55(19): 3751-3766.
[10] CUI Peng,ZHAO YiRen,YAO ZhiPeng,PANG LinJiang,LU GuoQuan. Starch Physicochemical Properties and Expression Levels of Anabolism Key Genes in Sweetpotato Under Low Temperature [J]. Scientia Agricultura Sinica, 2022, 55(19): 3831-3840.
[11] YuXia WEN,Jian ZHANG,Qin WANG,Jing WANG,YueHong PEI,ShaoRui TIAN,GuangJin FAN,XiaoZhou MA,XianChao SUN. Cloning, Expression and Anti-TMV Function Analysis of Nicotiana benthamiana NbMBF1c [J]. Scientia Agricultura Sinica, 2022, 55(18): 3543-3555.
[12] QU Cheng,WANG Ran,LI FengQi,LUO Chen. Cloning and Expression Profiling of Gustatory Receptor Genes BtabGR1 and BtabGR2 in Bemisia tabaci [J]. Scientia Agricultura Sinica, 2022, 55(13): 2552-2561.
[13] JIN MengJiao,LIU Bo,WANG KangKang,ZHANG GuangZhong,QIAN WanQiang,WAN FangHao. Light Energy Utilization and Response of Chlorophyll Synthesis Under Different Light Intensities in Mikania micrantha [J]. Scientia Agricultura Sinica, 2022, 55(12): 2347-2359.
[14] ZHANG Li,ZHANG Nan,JIANG HuQiang,WU Fan,LI HongLiang. Molecular Cloning and Expression Pattern Analysis of NPC2 Gene Family of Apis cerana cerana [J]. Scientia Agricultura Sinica, 2022, 55(12): 2461-2471.
[15] YUAN JingLi,ZHENG HongLi,LIANG XianLi,MEI Jun,YU DongLiang,SUN YuQiang,KE LiPing. Influence of Anthocyanin Biosynthesis on Leaf and Fiber Color of Gossypium hirsutum L. [J]. Scientia Agricultura Sinica, 2021, 54(9): 1846-1855.
Viewed
Full text


Abstract

Cited
  Shared   
  Discussed   
No Suggested Reading articles found!
京ICP备09089781号-30
Copyright 2018 © Editorial office of Scientia Agricultura Sinica
Tel: 86-010-82106279    E-mail: zgnykx@mail.caas.net.cn
Supported by Beijing Magtech Co.Ltd