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Acta Agronomica Sinica ›› 2022, Vol. 48 ›› Issue (11): 2934-2944.doi: 10.3724/SP.J.1006.2022.14243

• RESEARCH NOTES • Previous Articles     Next Articles

Interactions between CMLs and NPG1 and related proteins in pollen germination of Brassica oleracea L. var. capitata

XU Bin1,2(), CAO Shao-Yu1,2(), SU Tian1, PENG Meng-Ling1,2, LYU Xia1, LI Zhen-Lin1, ZHANG Guo-Ping1, XU Jun-Qiang1,*()   

  1. 1Dian-Tai Engineering Research Center for Characteristic Agriculture Industrialization of Yunnan Province, Yunnan Agricultural University, Kunming 650201, Yunnan, China
    2College of Landscape and Horticulture, Yunnan Agricultural University, Kunming 650201, Yunnan, China
  • Received:2021-12-22 Accepted:2022-03-25 Online:2022-11-12 Published:2022-04-20
  • Contact: XU Jun-Qiang E-mail:1650379536@qq.com;1194642629@qq.com;xujunqiang101@163.com
  • Supported by:
    The Major Projects of Yunnan Science and Technology Plan(202102AE09005);The Science and Technology Talents and Platform Plan of Yunnan Province(202205AF150017);The Science and Technology Talents and Platform Plan of Yunnan Province(202005AF150035);The Science and Technology Talents and Platform Plan of Yunnan Province(2019IC009);The National Natural Science Foundation of China(31560560);The Science and Technology Plan Project of Kunming(2019-1-H-24615)

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Abstract:

As one of calmodulin families, calmodulin-like (CMLs) regulate plant growth and development, hormone regulation, stresses, which have great significance to the further study of calmodulin-like protein involved in pollen germination and growth. In this study, to explore the interaction between CMLs and NPG1 related genes in pollen development of Brassica oleracea L. var. capitata, and to explore the function of CMLs in pollen development and germination, 12 CMLs genes related to pollen development and germination, and pollen germination genes NPG1, NPGR1, and NPGR2 were cloned from “ZG”. Interactions between them were detected by yeast two-hybrid test. and the relative expression levels of NPG1, NPGR1, and NPGR2 after different pollination time was detected. The results showed that the open reading frames (ORFs) of 12 CMLs genes ranged from 447 bp to 1095 bp, among which CML20, CML48, CML49, and CML50 contained 4 introns, CML21 contained 2 introns, and the others contained no introns. All of them contained no signal peptide and transmembrane domain, all of them were extracellular proteins and hydrophilic proteins which contain 2-4 EF-hands, with amino acids range of 148-364 aa. Subcellular localization was mainly located in cell membrane, vacuole, and nucleus. NPG1, NPGR1, and NPGR2 were clustered on different evolutionary branches, which were the closest to Brassica rape and Brassica napus, and closer to Arabidopsis thaliana. Yeast two-hybrid showed that CML13, CML21, CML24, CML42 could not interact with NPG1, NPGR1, and NPGR2 in vitro, CML15, CML20, CML25, CML39, CML41, CML48, and CML49 could interact with NPG1, NPGR1, and NPGR2, CML50 could interact with NPGR1 and NPGR2, but not with NPG1. The relative expression level of NPG1 increased significantly after pollination, while the relative expression levels of NPGR1 and NPGR2 didn’t change significantly. The relative expression levels of CMLs genes were varied at different pollination times, and CML15, CML20, CML39, CML41, and CML49 were a trend of first increasing and then decreasing. In conclusion, several CMLs proteins were screened which can interact with NPG1 and NPGRs, indicating that CMLs can participate in the process of pollen germination and pollen tube elongation, and it was expected to provide references for the research on the mechanism of Ca2+ signaling system participating in pollen germination and pollen tube elongation.

Key words: Brassica oleracea L. var. capitata, pollen, calmodulin-like protein (CMLs), NPG1, NPGRs, protein interaction

Table 1

Primers used in this study"

基因 Gene name 正向引物 Forward primer (5°-3°) 反向引物 Reverse primer (5°-3°)
CML13 GAGCGAAATCCGACCCGGCTT CTACTTAGCAACCATCCTGGCA
CML15 CTCTCATCTGTGTTTTGAGG TCATGAATTAATTTTTAAACCA
CML20 CGAGAAATCGACGCGGAAAGAGCT ATAACAGAGACCTCATCAGTACC
CML21 CGATCTGATCTCAAAGCAGGA CACAAACATCAAGCCTTGTCA
CML24 CATCGTCTTCTTCTCCACCACA CCTAAAATACGATCATCAAGC
CML25 GATCCAGAGATTCATTCGCTTCCTT GTGAAACTCTACCACTGACCAC
CML39 CATCATGAAGAACACTCAACGT CAACATTGGATGGGCTGATGCCTTA
CML41 CCAATATGGCAACTCCCCAAG CTTCATAAGCATTTCGAGCAA
CML42 GTCAAGGAAGAGGATAAATGG TGAAGTCAAGAAGGGATAACG
CML48 CTTGATGATGGGACTGGCAACACTG CATATGAGGCAATGAACGGAATGAC
CML49 ATGTCTGGTTACCCTCCTTCGAGC TTAAGCGACGAGGAACGGTAGAAC
CML50 TTCCCAGCGATGTCAGGTTACC GTTGTTGTTGTATGTTCGTCG
NPG1 GGCTCTGCATGAAAACAACTGA TTAAAGAATGGTTGAGAAGCT
NPGR1 ATGTTGTGTGCTTGTTCAGGCG TCAAATGAAACTCTGCACCGG
NPGR2 ATGAGGAACAGCGAGACTAGGC TCATCTGAATGGCTCCACTGGC
qCML15 CTCGGTCTCAAACCATCAGGAGA GTTACCGATCTCTTCGTTCAGG
qCML20 ATGTCGAGTCTATACAGAGGTG TGCTCTTCCGTCATCTCGAAACC
qCML25 GTTCGGCGTCTAGAACCGGAGCA TGGAACCTCGTGGCCTAGACTTG
qCML39 TCAAGACACTGGGAGAGCAA CAAAATCCAGCATCCCATCT
qCML41 GTCACCACTCCCATGACGAGCT TGCCTCGTGAGTTATATACTCAC
qCML48 TCAGCTTGATGATGGGACTG TAACCGGGGTCCTTCTCTTT
qCML49 GGAGACCACAAGCCGCACAAA CGCCTGGAAGCAAGTCACGAT
qCML50 ACCAACGCCATGAAGATAGG CATCTATTCTCCCGCTCCTG
qNPG1 TAGTCAGACCTCGGTGCTC GCTCCTCGCTGCAAACCTTA
qNPGR1 CGAATCAAGACAGATACCG CATAGCATACGCCAAGGAA
qNPGR2 AACTACGAGGAGGCGAGGGC GAGGCTGAGGAGGAGCAACA
β-Actin TATCAACTACCAGCCACC GAACACCTCAGCTACACTC

Fig. 1

Cloning of CMLs genes in Brassica oleracea L. var. capitata M: Trans2K plus II DNA marker; 1-12 represent the cloning of CML13, CML15, CML20, CML21, CML24, CML25, CML39, CML41, CML42,CML48, CML49, and CML50, respectively."

Table 2

Basic information of CMLs genes of Brassica oleracea L. var. capitata"

基因
Gene name		 编码区
Coding
region (bp)		 内含子
Introns		 跨膜域
Transmembrane		 信号肽
Signal peptide		 预测的蛋白 Predicted protein 疏水性
Hydrophobicity		 亚细胞定位
Subcellular
localization
EF-
hand		 氨基酸
Amino acid (aa)		 分子量
Molecular weight (kD)		 pI
CML13 447 0 无No 无No 3 148 16.40 4.62 亲水
Hydrophilic		 细胞膜
Cell membrane
CML15 471 0 无No 无No 4 156 16.99 3.94 亲水
Hydrophilic		 液泡
Vacuole
CML20 510 4 无No 无No 4 169 19.60 4.55 亲水
Hydrophilic		 细胞膜
Cell membrane
CML21 678 2 无No 无No 4 225 25.96 4.17 亲水
Hydrophilic		 细胞膜
Cell membrane
CML24 447 0 无No 无No 4 158 17.40 4.64 亲水
Hydrophilic		 细胞膜, 液泡
Cell membrane, vacuole
CML25 552 0 无No 无No 4 183 20.14 4.42 亲水
Hydrophilic		 液泡
Vacuole
CML39 510 0 无No 无No 4 169 19.25 4.35 亲水
Hydrophilic		 液泡
Vacuole
CML41 612 0 无No 无No 4 203 22.64 4.97 亲水
Hydrophilic		 细胞膜
Cell membrane
CML42 567 0 无No 无No 3 188 20.70 4.25 亲水
Hydrophilic		 细胞膜, 液泡
Cell membrane, vacuole
CML48 672 4 无No 无No 2 223 25.28 4.53 亲水
Hydrophilic		 细胞核
Nucleus
CML49 954 4 无No 无No 2 317 33.51 6.93 亲水
Hydrophilic		 细胞核
Nucleus
CML50 1095 4 无No 无No 2 364 38.06 6.27 亲水
Hydrophilic		 细胞膜, 细胞核
Cell membrane, nucleus

Fig. 2

Phylogenetic tree and gene structure of CMLs in Brassica oleracea L. var. capitata The phylogenetic tree is constructed on the left, and the gene structure map of the CMLs on the right."

Table 3

Basic information of NPG1, NPGR1, and NPGR2 of Brassica oleracea L. var. capitata"

基因
Gene		 编码区
Coding region
(bp)		 内含子
Introns		 跨膜域
Transmembrane		 信号肽
Signal peptide		 预测的蛋白 Predicted proteins 疏水性
Hydrophobicity		 亚细胞定位
Subcellular
localization
TPR 氨基酸
Amino
acid (aa)		 分子量Molecular
weight (kD)		 pI
NPG1 2043 4 无No 无No 3 680 75.31 5.98 亲水Hydrophilic 细胞核Nucleus
NPGR1 2109 2 无No 无No 3 702 77.65 6.27 亲水Hydrophilic 细胞核Nucleus
NPGR2 2224 3 无No 无No 7 737 82.44 7.58 亲水Hydrophilic 细胞核Nucleus

Fig. 3

Amplification and sequence analysis of NPG1, NPGR1, and NPGR2 genes in Brassica oleracea L. var. capitata M: Trans2K plus II DNA marker; A: amplification of NPG1, NPGR1 and NPGR2 genes from cDNA; B: amplification of NPG1, NPGR1, and NPGR2 genes from gDNA; C: analysis of TPRs domain of NPG1, NPGR1 and NPGR2 proteins in Brassica oleracea and Arabidopsis thaliana; D: sequence comparison of NPG1-TPR1 domain between Brassica oleracea, and Arabidopsis thaliana."

Fig. 4

Phylogenetic analysis of NPG1, NPGR1, and NPGR2 proteins in Brassica oleracea L. var. capitata"

Fig. 5

Autoactivation assay of the yeast strain by recombinant on SD/-Leu/-Trp/X-α-gal/AbA plates"

Table 4

Interaction of CMLs and NPG1, NPGR1, NPGR2 in Brassica oleracea L. var. capitata"

AD\BK CML13 CML15 CML20 CML21 CML24 CML25 CML39 CML41 CML42 CML48 CML49 CML50
NPG1 — + + — — + + + — + + —
NPGR1 — + + — — + + + — + + +
NPGR2 — + + — — + + + — + + +

Fig. 6

Interactions between CMLs and NPG1, NPGR1, NPGR2 in Brassica oleracea L. var. capitata P: positive control; N: negative control; 1: NPG1×CML13; 2: NPGR1×CML13; 3: NPGR2×CML13; 4: NPG1×CML15; 5: NPGR1×CML15; 6: NPGR2×CML15; 7: NPG1×CML20; 8: NPGR1×CML20; 9: NPGR2×CML20; 10: NPG1×CML21; 11: NPGR1×CML21; 12: NPGR2× CML21; 13: NPG1×CML24; 14: NPGR1×CML24; 15: NPGR2×CML24; 16: NPG1×CML25; 17: NPGR1×CML25; 18: NPGR2×CML25; 19: NPG1×CML39; 20: NPGR1×CML39; 21: NPGR2×CML39; 22: NPG1×CML41; 23: NPGR1×CML41; 24: NPGR2×CML41; 25: NPG1× CML42; 26: NPGR1 CML42; 27: NPGR2×CML42; 28: NPG1×CML48; 29: NPGR1×CML48; 30: NPGR2×CML48; 31: NPG1×CML49; 32: NPGR1×CML49; 33: NPGR2×CML49; 34: NPG1×CML50; 35: NPGR1×CML50; 36: NPGR2×CML50."

Table 5

Interaction strength of CMLs and NPG1, NPGR1, NPGR2 in Brassica oleracea L. var. capitata"

AD\BK β-半乳糖酶活性 β-galactosidase activity (Miller units)
CML15 CML20 CML25 CML39 CML41 CML48 CML49 CML50
NPG1 5.37 5.85 5.61 5.71 7.77 8.31 6.68 —
NPGR1 4.58 2.31 4.16 3.97 5.31 7.17 2.69 3.65
NPGR2 4.50 4.96 4.82 4.51 6.58 7.70 4.47 5.90

Fig. 7

Relative expression levels of CMLs (A), and NPG1, NPGR1, and NPGR2 (B) at different pollination times of Brassica oleracea L. var. capitata Different lowercase letter above the bar indicates significant difference at P < 0.05."

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