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

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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"

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