Scientia Agricultura Sinica ›› 2024, Vol. 57 ›› Issue (2): 390-402.doi: 10.3864/j.issn.0578-1752.2024.02.013

• ANIMAL SCIENCE·VETERINARY SCIENCE • Previous Articles     Next Articles

Cloning of PLZF Gene and Its Effects on the Proliferation of Undifferentiated Spermatogonia in Cattleyak

ZHANG Peng(), WANG MingXiu, JING KeMin, LI YuQian, TIAN Yuan, ZHONG JinCheng(), CAI Xin()   

  1. Key Laboratory of Qinghai-Tibetan Plateau Animal Genetic Resource Reservation and Utilization, Ministry of Education / Sichuan Province, Southwest Minzu University, Chengdu 610041
  • Received:2023-05-11 Accepted:2023-10-07 Online:2024-01-16 Published:2024-01-19
  • Contact: ZHONG JinCheng, CAI Xin

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Abstract:

【Objective】 As the product of interspecific hybridization between yak and cattle, cattleyak has excellent production performance, but the further application of its heterosis is limited by the male sterility of cattleyak. The aim of the study was to clone the PLZF of cattleyak, and to identify its differential expression in the testicular tissue and undifferentiated spermatogonia of cattleyak and yak, and to further reveal the effect of expressing this gene on the activity of undifferentiated spermatogonia of cattleyak. This study could provide a theoretical basis for clarifying the mechanism of spermatogenesis stagnation in cattleyaks. 【Method】 In this study, 24-month-old male Maiwa yak and F1 generation male cattleyak were used as experimental animals, and the CDS sequences of PLZF in cattleyak were cloned by RT-PCR and analyzed by bioinformatics. The differential expression of PZLF in the testis tissues of cattleyak and yak was analyzed by RT-qPCR. The expression vector of PLZF was constructed by homologous recombination, and the overexpression efficiency and the expression of downstream target genes were detected by RT-qPCR. The effect of overexpression of PLZF on the undifferentiated spermatogonia of cattleyak was detected by PDT, CCK-8, EdU, and immunofluorescence. 【Result】 The CDS region of the PLZF was cloned, and it was found by bioinformatics analysis that the protein sequence encoded by the gene did not contain transmembrane domain and signal peptide sequence, and its tertiary structure was mainly α helix and random curl. Phylogenetic tree analysis showed that the PLZF of cattleyak was more closely related to the PLZF of cattle. The prediction of tertiary structure showed that although the tertiary structure of PLZF protein of cattleyak, yak and cattle was highly similar, the PLZF protein of yak was quite different from that of cattleyak and cattle at amino acids 531-540. RT-qPCR found that the expression levels of PLZF gene in the testis tissue and undifferentiated spermatogonia of cattleyak were significantly lower than that in yak (P<0.05). After overexpression of PLZF, the expression of PLZF in the undifferentiated spermatogonia of the cattleyak was up-regulated by 13.8 times (P<0.01), and the proliferation activity of the undifferentiated spermatogonia of the cattleyak was significantly increased (P<0.05), which showed that the down-regulation of PLZF expression affected the proliferation activity of undifferentiated spermatogonia of cattleyak. In addition, after overexpression of PLZF, the proliferation activity of undifferentiated spermatogonia was significantly increased All proliferation-related genes (Etv5, Bcl6b, Pcna and c-fos) were significantly up-regulated (P<0.05), and all differentiation-related genes (Stra8, Kit, Dmrt1 and Sohlh2) were significantly down-regulated (P<0.05), indicating that PLZF could promote the proliferation of undifferentiated spermatogonia by up-regulating the expression of proliferation-related genes and down-regulating the expression of differentiation-related genes.【Conclusion】 The abnormal expression of PLZF in cattleyak undifferentiated spermatogonia reduced the proliferative activity of cattleyak undifferentiated spermatogonia, resulting in its decrease in number and affecting the spermatogenesis of cattleyak. This study provided a theoretical basis for further elucidation of the mechanism of spermatogenesis and stagnation in cattleyak, and a new idea for solving the problem of male sterility in cattleyak.

Key words: cattleyak, PLZF, undifferentiated spermatogonia, proliferation

Table 1

Primers for PLZF cloning"

基因 Gene 登录号 Accession NO. 引物序列 Primer sequence (5’→3’)
PLZF XM_005891907 F: CTAGCGTTTAAACTTAAGCTTATGGATCTGACAAAGATGGGCA
R: CCACACTGGACTAGTGGATCCTCACACGTAGCACAGATAGAGGTACG

Table 2

Primer sequence for RT-qPCR"

基因
Gene		 登录号
Accession No.		 引物序列
Primer sequences (5′→3′)		 引物长度
Primer Length (bp)		 退火温度
Tm (℃)		 产物长度
Product size (bp)
Bcl6b XM_005906036 F：GAAAACGCATAGCCGCATCC
R：GACTCTTGTGCCGGAAATGC		 20
20		 60.32
59.32		 248
Etv5 XM_005910750 F：ACCGGCAAATGTCAGAACCT
R：CGTCAAAGTACAACCGGGGA		 20
20		 59.89
59.97		 276
c-fos XM_005900989 F：GCCCGGACCTACAATGGCTA
R：CTCTGCCTCCTGTCATGGTTT		 20
21		 61.69
60.00		 150
Pcna XM_005906528 F：AGCTGAAGATAACGCAGACAC
R：ATCTCGGCATATACGTGCAA		 21
20		 58.39
57.19		 178
Dmrt1 XM_005900007 F：CCCGTGCCTGATGATTGAGA
R：GTACGGAAACAGAGACGGCT		 20
20		 59.82
59.76		 211
Sohlh2 XM_002691802 F：CTATCCGTCCCAGGCATGAT
R：ACCGATAGCCTTCTCTGACG		 20
20		 59.02
58.97		 189
Kit NM_001166484 F：AGAAAACGACACGCTGGTTC
R：CTCGCGCTTCACATTTCTGA		 20
20		 59.06
58.93		 151
Stra8 XM_005906930 F：TGTGGCAAGTTTCCTGGACA
R：TCTCCGTGCACCTCAACATT		 20
20		 59.74
59.60		 215
Plzf XM_005891907 F：GTTCCATGCCCACCGGACT
R：TGGCCTCCGTGTCATTGTCA		 19
20		 63.16
55.00		 275
β-actin DQ838049 F：CCCTGGAGAAGAGCTACGAG
R：TAGTTTCGTGAATGCCGCAG		 20
20		 58.97
58.92		 129

Table 3

Reaction program of RT-qPCR"

阶段
Stage		 循环数
Number of cycles		 温度
Temperature (℃)		 时间
Time
(s)
预变性Predenaturation 1 95 10
循环反应
Cyclic reaction		 40 95 10
60 30
溶解曲线
Melting curve		 1 95 15
60 60
95 15

Fig. 1

The amplification of the target fragment of PLZF of cattleyak P and M represent PLZF and Marker, respectively"

Table 4

Sequence comparison of CDS region of PLZF in different species"

物种
Specics		 登录号
Accession No.		 CDS区长度
Length of CDS region (bp)		 相似性
Percent identity (%)
牦牛 Bos Mutus XM_005891907 2 019 98.96
黄牛 Bos Taurus XM_005215851 2 022 99.80
瘤牛 Bos indicus XM_019974560 2 022 99.75
猪 Sus scrofa XM_021062870 2 022 94.07
山羊 Capra hircus XM_018058857 2 022 97.23

Fig. 2

Sequence comparison of CDS region of PLZF in different species"

Fig. 3

Characteristic information analysis, structural analysis and phylogenetic tree of PLZF protein of cattleyak (A) Prediction analysis of transmembrane structure domain. (B) Prediction analysis of hydrophobicity and hydrophilicity. (C) Signal peptide sequence prediction analysis. (D) Prediction analysis of secondary structure in protein. (E) The phylogenetic tree of PLZF gene sequence"

Fig. 4

Tertiary structure prediction and protein structure difference analysis of PLZF protein in cattleyak, yak and cattle (A-B) Analysis of amino acid sequence differences of PLZF among cattleyak, yak and cattle. (C-E) Prediction of tertiary structure of PLZF protein in cattle, yak and cattleyak. (F-K) Analysis of structural differences of PLZF protein among cattle, yak and cattleyak"

Fig. 5

Expression of PLZF in testis of yak and cattleyak YK represents yak, CY represents cattleyak (the same below). ** means P<0.01"

Fig. 6

Identification of PLZF expression vector by enzyme digestion and overexpression efficiency (A) Identification of PLZF expression vector by enzyme digestion. M, 1, 2, and 3 represent Marker, expression vector by double enzyme digestion, PLZF gene cloning, and linear pcDNA3.1(+) empty vector, respectively. (B) PLZF gene overexpression efficiency. Bars that do not share the same letters are significantly different from each other (P<0.05). CY-PLZF represents the overexpression of PLZF gene in the undifferentiated spermatogonia of cattleyak. The same as below"

Fig. 7

Effect of overexpression of PLZF gene on undifferentiated spermatogonia of cattleyak A: Population doubling times of the cells for YK, CY-PLZF and CY groups; B: The proliferation of YK, CY-PLZF, CY-TAF4b and CY was detected by CCK-8 under different conditions; C: Proliferation of CY, CY-PLZF and YK undifferentiated spermatogonia were detected by EdU. Red image indicates “EdU”, blue image indicates “H33342”, and “Merge” indicated the merged image; D: Proliferation of CY, CY-PLZF and YK undifferentiated spermatogonia were detected by immunofluorescence of DDX4. Green image indicated “DDX4”, blue image indicated “DAPI”, and “Merge” indicated the merged image"

Fig. 8

Expression of PLZF target genes in undifferentiated spermatogonia of cattleyak"

Fig. 9

Effects of PLZF on proliferation of undifferentiated spermatogonia in cattleyak"

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