Scientia Agricultura Sinica ›› 2024, Vol. 57 ›› Issue (24): 4839-4853.doi: 10.3864/j.issn.0578-1752.2024.24.002

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Identification of Alfalfa (Medicago sativa) MsCEP Genes and Functional Analysis of Its Regulation in Root Growth and Development

ZENG XiangCui1(), YANG YongNian1,2, LI RuYue1, JIANG XueQian1, JIANG Xu1, XU YanRan1, LIU ZhongKuan3, LONG RuiCai1, KANG JunMei1, YANG QingChuan1, LI MingNa1()   

  1. 1 Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100193
    2 College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou 510642
    3 Institute of Agricultural Resources and Environment Research, Hebei Academy of Agriculture and Forestry Sciences, Shijiazhuang 050051
  • Received:2024-05-31 Accepted:2024-07-12 Online:2024-12-16 Published:2024-12-23
  • Contact: LI MingNa

Abstract:

【Objective】CEP (C-terminal encoded peptides) is a gene that encodes hormone-like peptides secreted by roots and serves as a key regulator of plant root growth and development. To provide a molecular theoretical basis for further elucidating the function of MsCEP genes in root growth and development, members of the Medicago sativa MsCEP gene family, basic characteristics, expression differences in different tissues, and their roles in root growth were identified and analyzed. 【Method】Based on the genomic information of the alfalfa cultivar Xinjiang Daye, the MsCEP gene family members of alfalfa were accurately identified using local Blast analysis in TBtools and feature domain by referring to MtCEP family protein of Medicago truncatula sequence. The fundamental genetic and protein characteristics and the phylogenetic relationship of the MsCEP genes were analyzed by bioinformatics methods. The expression patterns of alfalfa MsCEP gene family members in various tissues were assessed using transcriptome data and real-time fluorescence quantitative PCR. The functional roles of mature MsCEP peptides in root growth and development were analyzed by exogenous application experiments. 【Result】A total of 35 MsCEP family members were identified in the genome of alfalfa Xinjiang Daye, and these genes are distributed across 18 chromosomes, lack introns, and all possess an N-terminal signal peptide and one or two conserved domains of the CEP family. The MsCEP members displayed predicted amino acid length ranging from 59 to 150, with molecular weights spanning 6.7 to 16.2 kDa, the isoelectric points varying from 5.80 to 10.41, instability indices ranging from 30.63 to 89.93, aliphatic indices ranging from 54.41 to 134.88, and the grand average of hydropathicity ranging from -1.110 to 0.377. Subcellular localization predictions indicated that the MsCEP protein predominantly localizes to the nucleus, plasma membrane, chloroplast, and Golgi apparatus. Cluster analysis delineated three distinct branches within the family, aligning with counterparts from Arabidopsis thaliana and Medicago truncatula. The largest branch encompassed 48 CEP members. Collinearity analysis highlighted a collinear relationship between the MsCEP genes in alfalfa and those in Arabidopsis thaliana and Medicago truncatula. Tissue expression analysis revealed that members of the MsCEP family exhibit distinct tissue-specific expression patterns, with higher expression levels in roots and lower or no expression detected in leaves. Among them, 22 members exhibited higher expression levels in roots compared to other tissues. The exogenous application of synthetic mature MsCEP2 peptide suppressed the growth of primary and lateral roots, reduced the number of lateral roots, and decreased the density of lateral roots. 【Conclusion】In conclusion, our investigation identified a total of 35 MsCEP members from the alfalfa 'Xinjiangdaye' genome database, which are revealed to be highly conserved. The MsCEP genes are primarily expressed in roots, and the exogenous application of synthetic mature MsCEP peptides can regulate root morphology, indicating that MsCEP peptides play important roles in root growth and development of alfalfa.

Key words: alfalfa, MsCEP gene family, CEP2, exogenous application of peptide, root growth and development

Table 1

The physiochemical characteristics of 35 members in the alfalfa MsCEP gene family"

基因编号
Gene ID
基因名称
Gene name
氨基酸数目
No. of amino acids
等电点
pI
分子量
Molecular weight (Da)
不稳定指数
Instability
index
脂肪系数
Aliphatic
index
平均疏水指数
Grand average of hydropathicity
亚细胞定位
Subcellular localization
MS.gene24367.t1 MsCEP1 107 6.40 12077.73 37.90 81.96 -0.428 细胞核Nucleus
MS.gene044007.t1 MsCEP2 107 5.86 12066.66 43.06 83.83 -0.407 细胞核Nucleus
MS.gene67093.t1 MsCEP3 107 5.86 12066.66 43.06 83.83 -0.407 细胞核Nucleus
MS.gene062764.t1 MsCEP4 107 5.86 12066.66 43.06 83.83 -0.407 细胞核Nucleus
MS.gene63725.t1 MsCEP5 86 10.41 9234.91 36.16 134.88 0.377 叶绿体Chloroplast
MS.gene002621.t1 MsCEP6 102 9.75 11158.06 52.67 99.31 -0.079 高尔基体、细胞核
Golgi apparatus, Nucleus
MS.gene01607.t1 MsCEP7 102 9.75 11158.06 52.67 99.31 -0.079 高尔基体、细胞核
Golgi apparatus, Nucleus
MS.gene03109.t1 MsCEP8 102 9.75 11145.06 52.67 99.31 -0.052 细胞核Nucleus
MS.gene004299.t1 MsCEP9 102 9.75 11144.03 48.89 99.31 -0.079 细胞核Nucleus
MS.gene049393.t1 MsCEP10 90 5.80 9926.39 61.99 79.11 -0.162 叶绿体、细胞核Chloroplast, Nucleus
MS.gene06520.t1 MsCEP11 90 5.80 9926.39 61.99 79.11 -0.162 叶绿体、细胞核Chloroplast, Nucleus
MS.gene013422.t1 MsCEP12 90 5.80 9926.39 61.99 79.11 -0.162 叶绿体、细胞核Chloroplast, Nucleus
MS.gene27830.t1 MsCEP13 99 10.11 10829.94 54.09 105.25 0.193 叶绿体、高尔基体、细胞核
Chloroplast, Golgi apparatus, Nucleus
MS.gene058837.t1 MsCEP14 99 10.11 10829.94 54.09 105.25 0.193 叶绿体、高尔基体、细胞核
Chloroplast, Golgi apparatus, Nucleus
MS.gene023603.t1 MsCEP15 99 10.11 10829.94 54.09 105.25 0.193 叶绿体、高尔基体、细胞核Chloroplast, Golgi apparatus, Nucleus
MS.gene28597.t1 MsCEP16 141 7.87 15729.38 41.08 60.14 -0.755 细胞核Nucleus
MS.gene28596.t1 MsCEP17 102 6.96 10651.16 50.09 98.43 0.108 细胞膜、细胞核Cell membrane, Nucleus
MS.gene44917.t1 MsCEP18 141 7.87 15743.4 42.15 60.14 -0.755 细胞核Nucleus
MS.gene44918.t1 MsCEP19 102 6.96 10651.16 50.09 98.43 0.108 细胞膜、细胞核Cell membrane, Nucleus
MS.gene44919.t1 MsCEP20 150 10.23 16286.74 31.10 68.80 -0.382 细胞膜Cell membrane
MS.gene82945.t1 MsCEP21 63 8.23 6692.53 89.93 63.49 -0.606 细胞核Nucleus
MS.gene011842.t1 MsCEP22 141 7.87 15743.4 42.15 60.14 -0.755 细胞核Nucleus
MS.gene011843.t1 MsCEP23 102 6.96 10651.16 50.09 98.43 0.108 细胞膜、细胞核Cell membrane, Nucleus
MS.gene011844.t1 MsCEP24 150 10.23 16286.74 31.10 68.8 -0.382 细胞膜Cell membrane
MS.gene056566.t1 MsCEP25 63 8.23 6722.56 84.82 61.90 -0.646 细胞核Nucleus
MS.gene80019.t1 MsCEP26 90 5.86 9511.51 52.70 70.44 -0.607 细胞核Nucleus
MS.gene80020.t1 MsCEP27 141 7.87 15743.4 42.15 60.14 -0.755 细胞核Nucleus
MS.gene80021.t1 MsCEP28 122 9.69 13361.94 30.63 65.33 -0.517 细胞核Nucleus
MS.gene80022.t1 MsCEP29 150 10.19 16238.65 31.23 68.80 -0.397 细胞膜Cell membrane
MS.gene067991.t1 MsCEP30 63 8.23 6722.56 84.82 61.90 -0.646 细胞核Nucleus
MS.gene28559.t1 MsCEP31 59 10.04 6739.56 72.42 54.41 -1.110 细胞核Nucleus
MS.gene28558.t1 MsCEP32 150 10.23 16286.74 31.10 68.80 -0.382 细胞膜Cell membrane
MS.gene28557.t1 MsCEP33 102 6.96 10651.16 50.09 98.43 0.108 细胞膜、细胞核Cell membrane, Nucleus
MS.gene28556.t1 MsCEP34 141 7.06 15716.33 39.26 58.79 -0.772 细胞核Nucleus
MS.gene83398.t1 MsCEP35 63 8.23 6722.56 84.82 61.90 -0.646 细胞核Nucleus

Fig. 1

The distribution of MsCEP gene family on alfalfa chromosomes"

Fig. 2

Gene structures of MsCEP genes in alfalfa"

Fig. 3

The conserved motifs of MsCEP proteins in alfalfa A: Alignment of conserved motifs of MsCEP proteins; B: The consensus sequence of CEP motifs in Arabidopsis, Medicago truncatula and Medicago sativa; C: The N-terminal signal peptide cleavage site of MsCEP proteins"

Fig. 4

Phylogenetic analysis of CEP proteins from Arabidopsis, Medicago truncatula and Medicago sativa"

Fig. 5

Syntenic relationships of CEP gene family in Arabidopsis, Medicago truncatula and Medicago sativa A: Syntenic relationships of MsCEP and MtCEP; B: Syntenic relationships of MsCEP and AtCEP"

Fig. 6

Cis-acting elements of the promoters in alfalfa MsCEP family genes"

Fig. 7

The expression patterns of MsCEP gene family in different tissues A: The expression heatmap of CEP gene family in different tissues; B: The expression patterns of MsCEP2 in different tissues of ten-day-old seedling and four-week-old seedling. Different letters in the figures represent significant difference at P<0.05"

Fig. 8

The root phenotype analysis of Arabidopsis thaliana treated with mature peptide MsCEP2 A: Absorption of mature peptide MsCEP2 by Arabidopsis thaliana; B: Phenotype of Arabidopsis thaliana treated with mature peptide MsCEP2 for seven days; C: Phenotypic analysis of root systems of Arabidopsis thaliana treated with mature peptide MsCEP2 for seven days. ** represent significant difference at P<0.01"

[1]
CHEN L, HE F, LONG R C, ZHANG F, LI M N, WANG Z, KANG J M, YANG Q C. A global alfalfa diversity panel reveals genomic selection signatures in Chinese varieties and genomic associations with root development. Journal of Integrative Plant Biology, 2021, 63(11): 1937-1951.

doi: 10.1111/jipb.13172
[2]
RADOVIC J, SOKOLOVIC D, MARKOVIC J. Alfalfa-most important perennial forage legume in animal husbandry. Biotechnology in Animal Husbandry, 2009, 25(5/6): 465-475.
[3]
DELAY C, IMIN N, DJORDJEVIC M A. CEP genes regulate root and shoot development in response to environmental cues and are specific to seed plants. Journal of Experimental Botany, 2013, 64(17): 5383-5394.

doi: 10.1093/jxb/ert332 pmid: 24179096
[4]
ROBERTS I, SMITH S, DE RYBEL B, VAN DEN BROEKE J, SMET W, DE COKERE S, MISPELAERE M, DE SMET I, BEECKMAN T. The CEP family in land plants: evolutionary analyses, expression studies, and role in Arabidopsis shoot development. Journal of Experimental Botany, 2013, 64(17): 5371-5381.
[5]
TALESKI M, IMIN N, DJORDJEVIC M A. CEP peptide hormones: key players in orchestrating nitrogen-demand signalling, root nodulation, and lateral root development. Journal of Experimental Botany, 2018, 69(8): 1829-1836.

doi: 10.1093/jxb/ery037 pmid: 29579226
[6]
AGGARWAL S, KUMAR A, JAIN M, SUDAN J, SINGH K, KUMARI S, MUSTAFIZ A. C-terminally encoded peptides (CEPs) are potential mediators of abiotic stress response in plants. Physiology and Molecular Biology of Plants: An International Journal of Functional Plant Biology, 2020, 26(10): 2019-2033.
[7]
SMITH S, ZHU S S, JOOS L, ROBERTS I, NIKONOROVA N, VU L D, STES E, CHO H, LARRIEU A, XUAN W, GOODALL B, VAN DE COTTE B, WAITE J M, RIGAL A, HARBOROUGH S R, PERSIAU G, VANNESTE S, KIRSCHNER G K, VANDERMARLIERE E, MARTENS L, STAHL Y, AUDENAERT D, FRIML J, FELIX G, SIMON R, BENNETT M J, BISHOPP A, DE JAEGER G, LJUNG K, KEPINSKI S, ROBERT S, NEMHAUSER J, HWANG I, GEVAERT K, BEECKMAN T, DE SMET I. The CEP5 peptide promotes abiotic stress tolerance, As revealed by quantitative proteomics, and attenuates the AUX/IAA equilibrium in Arabidopsis. Molecular & Cellular Proteomics, 2020, 19(8): 1248-1262.
[8]
MURPHY E, SMITH S, DE SMET I. Small signaling peptides in Arabidopsis development: How cells communicate over a short distance. The Plant Cell, 2012, 24(8): 3198-3217.
[9]
MATSUBAYASHI Y. Post-translational modifications in secreted peptide hormones in plants. Plant & Cell Physiology, 2011, 52(1): 5-13.
[10]
TABATA R, SUMIDA K, YOSHII T, OHYAMA K, SHINOHARA H, MATSUBAYASHI Y. Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science, 2014, 346(6207): 343-346.

doi: 10.1126/science.1257800 pmid: 25324386
[11]
CHU H W, LIANG W Q, LI J, HONG F, WU Y F, WANG L K, WANG J, WU P, LIU C M, ZHANG Q F, XU J, ZHANG D B. A CLE-WOX signalling module regulates root meristem maintenance and vascular tissue development in rice. Journal of Experimental Botany, 2013, 64(17): 5359-5369.

doi: 10.1093/jxb/ert301 pmid: 24043854
[12]
CHEN J, YU F, LIU Y, DU C Q, LI X S, ZHU S R, WANG X C, LAN W Z, RODRIGUEZ P L, LIU X M, LI D P, CHEN L B, LUAN S. FERONIA interacts with ABI2-type phosphatases to facilitate signaling cross-talk between abscisic acid and RALF peptide in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 2016, 113(37): E5519-E5527.
[13]
ZHANG X X, LIU W J, NAGAE T T, TAKEUCHI H, ZHANG H Q, HAN Z F, HIGASHIYAMA T, CHAI J J. Structural basis for receptor recognition of pollen tube attraction peptides. Nature Communications, 2017, 8(1): 1331.

doi: 10.1038/s41467-017-01323-8 pmid: 29109411
[14]
AN Z C, LIU Y L, OU Y, LI J, ZHANG B W, SUN D Y, SUN Y, TANG W Q. Regulation of the stability of RGF1 receptor by the ubiquitin-specific proteases UBP12/UBP13 is critical for root meristem maintenance. Proceedings of the National Academy of Sciences of the United States of America, 2018, 115(5): 1123-1128.
[15]
ZHU Q K, SHAO Y M, GE S T, ZHANG M M, ZHANG T S, HU X T, LIU Y D, WALKER J, ZHANG S Q, XU J. A MAPK cascade downstream of IDA-HAE/HSL2 ligand-receptor pair in lateral root emergence. Nature Plants, 2019, 5(4): 414-423.

doi: 10.1038/s41477-019-0396-x pmid: 30936437
[16]
黎家, 李传友. 新中国成立70年来植物激素研究进展. 中国科学(生命科学), 2019, 49(10): 1227-1281.
LI J, LI C Y. Seventy-year major research progress in plant hormones by Chinese scholars. Scientia Sinica (Vitae), 2019, 49(10): 1227-1281. (in Chinese)
[17]
OHYAMA K, OGAWA M, MATSUBAYASHI Y. Identification of a biologically active, small, secreted peptide in Arabidopsis by in silico gene screening, followed by LC-MS-based structure analysis. The Plant Journal, 2008, 55(1): 152-160.
[18]
DE BANG T C, LUNDQUIST P K, DAI X B, BOSCHIERO C, ZHUANG Z H, PANT P, TORRES-JEREZ I, ROY S, NOGALES J, VEERAPPAN V, DICKSTEIN R, UDVARDI M K, ZHAO P X, SCHEIBLE W R. Genome-wide identification of Medicago peptides involved in macronutrient responses and nodulation. Plant Physiology, 2017, 175(4): 1669-1689.
[19]
LEBEDEVA M A, GANCHEVA M S, KULAEVA O A, ZORIN E A, DOBYCHKINA D A, ROMANYUK D A, SULIMA A S, ZHUKOV V A, LUTOVA L A. Identification and expression analysis of the C-TERMINALLY ENCODED PEPTIDE family in Pisum sativum L.. International Journal of Molecular Sciences, 2022, 23(23): 14875.
[20]
ZHANG L, REN Y, XU Q, WAN Y M, ZHANG S Z, YANG G D, HUANG J G, YAN K, ZHENG C C, WU C G. SiCEP3, a C-terminally encoded peptide from Setaria italica, promotes ABA import and signaling. Journal of Experimental Botany, 2021, 72(18): 6260-6273.
[21]
DELAY C, CHAPMAN K, TALESKI M, WANG Y W, TYAGI S, XIONG Y, IMIN N, DJORDJEVIC M A. CEP3 levels affect starvation-related growth responses of the primary root. Journal of Experimental Botany, 2019, 70(18): 4763-4774.

doi: 10.1093/jxb/erz270 pmid: 31173100
[22]
ROBERTS I, SMITH S, STES E, DE RYBEL B, STAES A, VAN DE COTTE B, NJO M F, DEDEYNE L, DEMOL H, LAVENUS J, AUDENAERT D, GEVAERT K, BEECKMAN T, DE SMET I. CEP5 and XIP1/CEPR1 regulate lateral root initiation in Arabidopsis. Journal of Experimental Botany, 2016, 67(16): 4889-4899.
[23]
TALESKI M, CHAPMAN K, NOVÁK O, SCHMÜLLING T, FRANK M, DJORDJEVIC M A. CEP peptide and cytokinin pathways converge on CEPD glutaredoxins to inhibit root growth. Nature Communications, 2023, 14(1): 1683.

doi: 10.1038/s41467-023-37282-6 pmid: 36973257
[24]
CHAPMAN K, TALESKI M, FRANK M, DJORDJEVIC M A. C-terminally encoded peptide (cep) and cytokinin hormone signaling intersect to promote shallow lateral root angles. Journal of Experimental Botany, 2024, 75(2): 631-641.
[25]
PATEL N, MOHD-RADZMAN N A, CORCILIUS L, CROSSETT B, CONNOLLY A, CORDWELL S J, IVANOVICI A, TAYLOR K, WILLIAMS J, BINOS S, MARIANI M, PAYNE R J, DJORDJEVIC M A. Diverse peptide hormones affecting root growth identified in the Medicago truncatula secreted peptidome. Molecular & Cellular Proteomics, 2018, 17(1): 160-174.
[26]
IMIN N, MOHD-RADZMAN N A, OGILVIE H A, DJORDJEVIC M A. The peptide-encoding CEP1 gene modulates lateral root and nodule numbers in Medicago truncatula. Journal of Experimental Botany, 2013, 64(17): 5395-5409.
[27]
ZHU F G, DENG J, CHEN H, LIU P, ZHENG L H, YE Q Y, LI R, BRAULT M, WEN J Q, FRUGIER F, DONG J L, WANG T. A CEP peptide receptor-like kinase regulates auxin biosynthesis and ethylene signaling to coordinate root growth and symbiotic nodulation in Medicago truncatula. The Plant Cell, 2020, 32(9): 2855-2877.
[28]
ZHU F G, YE Q Y, CHEN H, DONG J L, WANG T. Multigene editing reveals that MtCEP1/2/12 redundantly control lateral root and nodule number in Medicago truncatula. Journal of Experimental Botany, 2021, 72(10): 3661-3676.
[29]
CHEN C J, CHEN H, ZHANG Y, THOMAS H R, FRANK M H, HE Y H, XIA R. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Molecular Plant, 2020, 13(8): 1194-1202.

doi: S1674-2052(20)30187-8 pmid: 32585190
[30]
CHEN H T, ZENG Y, YANG Y Z, HUANG L L, TANG B L, ZHANG H, HAO F, LIU W, LI Y H, LIU Y B, ZHANG X S, ZHANG R, ZHANG Y S, LI Y X, WANG K, HE H, WANG Z K, FAN G Y, YANG H, BAO A K, SHANG Z H, CHEN J H, WANG W, QIU Q. Allele-aware chromosome-level genome assembly and efficient transgene-free genome editing for the autotetraploid cultivated alfalfa. Nature Communications, 2020, 11(1): 2494.

doi: 10.1038/s41467-020-16338-x pmid: 32427850
[31]
CHAO J T, KONG Y Z, WANG Q, SUN Y H, GONG D P, LV J, LIU G S. MapGene2Chrom, a tool to draw gene physical map based on Perl and SVG languages. Hereditas, 2015, 37(1): 91-97.
[32]
DUVAUD S, GABELLA C, LISACEK F, STOCKINGER H, IOANNIDIS V, DURINX C. Expasy, the Swiss Bioinformatics Resource Portal, as designed by its users. Nucleic Acids Research, 2021, 49(W1): W216-W227.

doi: 10.1093/nar/gkab225 pmid: 33849055
[33]
CHOU K C, SHEN H B. Plant-mPLoc: A top-down strategy to augment the power for predicting plant protein subcellular localization. PLoS ONE, 2010, 5(6): e11335.
[34]
TEUFEL F, ALMAGRO ARMENTEROS J J, JOHANSEN A R, GÍSLASON M H, PIHL S I, TSIRIGOS K D, WINTHER O, BRUNAK S, VON HEIJNE G, NIELSEN H. SignalP 6.0 predicts all five types of signal peptides using protein language models. Nature Biotechnology, 2022, 40(7): 1023-1025.

doi: 10.1038/s41587-021-01156-3 pmid: 34980915
[35]
TAMURA K, STECHER G, KUMAR S. MEGA11: Molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 2021, 38(7): 3022-3027.

doi: 10.1093/molbev/msab120 pmid: 33892491
[36]
LETUNIC I, BORK P. Interactive Tree of Life (iTOL) v6: Recent updates to the phylogenetic tree display and annotation tool. Nucleic Acids Research, 2024, 52(W1): W78-W82.
[37]
WANG Y P, TANG H B, DEBARRY J D, TAN X, LI J P, WANG X Y, LEE T H, JIN H Z, MARLER B, GUO H, KISSINGER J C, PATERSON A H. MCScanX: A toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Research, 2012, 40(7): e49.
[38]
LESCOT M, DÉHAIS P, THIJS G, MARCHAL K, MOREAU Y, VAN DE PEER Y, ROUZÉ P, ROMBAUTS S. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research, 2002, 30(1): 325-327.
[39]
O’ROURKE J A, FU F L, BUCCIARELLI B, YANG S S, SAMAC D A, LAMB J F S, MONTEROS M J, GRAHAM M A, GRONWALD J W, KROM N, LI J, DAI X B, ZHAO P X, VANCE C P. The Medicago sativa gene index 1.2: A web-accessible gene expression atlas for investigating expression differences between Medicago sativa subspecies. BMC Genomics, 2015, 16(1): 502.
[40]
LI R, AN J P, YOU C X, SHU J, WANG X F, HAO Y J. Identification and expression of the CEP gene family in apple (Malus×domestica). Journal of Integrative Agriculture, 2018, 17(2): 348-358.
[41]
潘小婷, 张静, 葛廷, 马岩岩, 邓烈, 何绍兰, 易时来, 郑永强, 吕强, 谢让金. 柑橘CitCEP基因家族的鉴定及对逆境和激素的响应. 中国农业科学, 2018, 51(16): 3147-3158. doi: 10.3864/j.issn.0578-1752.2018.16.010.
PAN X T, ZHANG J, GE T, MA Y Y, DENG L, HE S L, YI S L, ZHENG Y Q, Q, XIE R J. Identification of Citrus CitCEP genes and their transcriptional response to stress and hormone treatments. Scientia Agricultura Sinica, 2018, 51(16): 3147-3158. doi: 10.3864/j.issn.0578-1752.2018.16.010. (in Chinese)
[42]
JEON J E, KIM J G, FISCHER C R, MEHTA N, DUFOUR- SCHROIF C, WEMMER K, MUDGETT M B, SATTELY E. A pathogen-responsive gene cluster for highly modified fatty acids in tomato. Cell, 2020, 180(1): 176-187.

doi: S0092-8674(19)31322-4 pmid: 31923394
[43]
FAN P X, WANG P P, LOU Y R, LEONG B J, MOORE B M, SCHENCK C A, COMBS R, CAO P F, BRANDIZZI F, SHIU S H, LAST R L. Evolution of a plant gene cluster in Solanaceae and emergence of metabolic diversity. eLife, 2020, 9: e56717.
[44]
OWJI H, NEZAFAT N, NEGAHDARIPOUR M, HAJIEBRAHIMI A, GHASEMI Y. A comprehensive review of signal peptides: Structure, roles, and applications. European Journal of Cell Biology, 2018, 97(6): 422-441.

doi: S0171-9335(18)30018-9 pmid: 29958716
[45]
VON HEIJNE G. Signal sequences. Journal of Molecular Biology, 1985, 184(1): 99-105.
[46]
RUDHE C, CLIFTON R, WHELAN J, GLASER E. N-terminal domain of the dual-targeted pea glutathione reductase signal peptide controls organellar targeting efficiency. Journal of Molecular Biology, 2002, 324(4): 577-585.

doi: 10.1016/s0022-2836(02)01133-6 pmid: 12460562
[47]
LAFFONT C, FRUGIER F. Rhizobium symbiotic efficiency meets CEP signaling peptides. The New Phytologist, 2024, 241(1): 24-27.
[1] CHEN FeiEr, ZHANG ZhiPeng, JIANG QingXue, MA Lin, WANG XueMin. Cloning and Biological Function Verification of Alfalfa MsSPL17 [J]. Scientia Agricultura Sinica, 2024, 57(17): 3335-3349.
[2] ZHAO JianTao, YANG KaiXin, WANG XuZhe, MA ChunHui, ZHANG QianBing. Effect of Phosphorus Application on Physiological Parameters and Antioxidant Capacity in Alfalfa Leaves [J]. Scientia Agricultura Sinica, 2023, 56(3): 453-465.
[3] SU Qian,DU WenXuan,MA Lin,XIA YaYing,LI Xue,QI Zhi,PANG YongZhen. Cloning and Functional Analyses of MsCIPK2 in Medicago sativa [J]. Scientia Agricultura Sinica, 2022, 55(19): 3697-3709.
[4] ZHANG YunXiu,JIANG Xu,WEI ChunXue,JIANG XueQian,LU DongYu,LONG RuiCai,YANG QingChuan,WANG Zhen,KANG JunMei. The Functional Analysis of High Mobility Group MsHMG-Y Involved in Flowering Regulation in Medicago sativa L. [J]. Scientia Agricultura Sinica, 2022, 55(16): 3082-3092.
[5] MA Lin,WEN HongYu,WANG XueMin,GAO HongWen,PANG YongZhen. Cloning and Function Analysis of MsMAX2 Gene in Alfalfa (Medicago sativa L.) [J]. Scientia Agricultura Sinica, 2021, 54(19): 4061-4069.
[6] ZeMin LI,Chen ZHANG,ChongYu ZHANG,GuiGuo ZHANG. The Relationship Between Nutrients and Biological Yield of Different Varieties of Alfalfa [J]. Scientia Agricultura Sinica, 2020, 53(6): 1269-1277.
[7] KANG JunMei,ZHANG QiaoYan,JIANG Xu,WANG Zhen,ZHANG TieJun,LONG RuiCai,CUI HuiTing,YANG QingChuan. Cloning MsSQE1 from Alfalfa and Functional Analysis in Saponin Synthesis [J]. Scientia Agricultura Sinica, 2020, 53(2): 247-260.
[8] JIANG Xu,CUI HuiTing,WANG Zhen,ZHANG TieJun,LONG RuiCai,YANG QingChuan,KANG JunMei. Cloning and Function Analysis of MsNST in Lignin and Cellulose Biosynthesis Pathway from Alfalfa [J]. Scientia Agricultura Sinica, 2020, 53(18): 3818-3832.
[9] LIU JiaoJiao,WANG XueMin,MA Lin,CUI MiaoMiao,CAO XiaoYu,ZHAO Wei. Isolation, Identification, and Response to Abiotic Stress of MsWRKY42 Gene from Medicago sativa L. [J]. Scientia Agricultura Sinica, 2020, 53(17): 3455-3466.
[10] GONG Hao,YANG Liu,LI DanDan,LIU GuoFu,XIAO ZhiXin,WU QingYing,CUI GuoWen. Response of Alfalfa Production and Quality to Fertilization and Cutting Frequency and Benefit Analysis in Mollisol Agricultural Area in Cold Region [J]. Scientia Agricultura Sinica, 2020, 53(13): 2657-2667.
[11] XIAO ZhiXin,WANG Yang,LIU GuoFu,GONG Hao,LI DanDan,GONG Lin,BAI ZhenJian,CUI GuoWen. Effects of Fertilizing Time in Early Spring on Alfalfa (Medicago sativa) Production Performance and Nutritional Quality in Mollisol Area in Cold Region [J]. Scientia Agricultura Sinica, 2020, 53(13): 2668-2677.
[12] XiaoDong LI,YiShun SHANG,ShiGe LI,GuangJi CHEN,ChengJiang PEI,Fang SUN,XianQin XIONG. The Mechanism of Ectopic Expression of Brassica juncea Multidrug and Toxic Compound Extrusion (BjMATE) to Enhance the Resistance to Acid and Aluminum Stress in Alfalfa [J]. Scientia Agricultura Sinica, 2020, 53(1): 18-28.
[13] SUN JuanJuan, A LaMuSi, ZHAO JinMei, XUE YanLin, YU LinQing, YU Zhu, ZHANG YingJun. Analysis of Amino Acid Composition and Six Native Alfalfa Cultivars [J]. Scientia Agricultura Sinica, 2019, 52(13): 2359-2367.
[14] SUN YanMei,ZHANG QianBing,MIAO XiaoRong,LIU JunYing,YU Lei,MA ChunHui. Effects of Phosphorus-Solubilizing Bacteria and Arbuscular Mycorrhizal Fungi on Production Performance and Root Biomass of Alfalfa [J]. Scientia Agricultura Sinica, 2019, 52(13): 2230-2242.
[15] ZHANG CuiMei, SHI ShangLi, WU Fang. Effects of Drought Stress on Root and Physiological Responses of Different Drought-Tolerant Alfalfa Varieties [J]. Scientia Agricultura Sinica, 2018, 51(5): 868-882.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
No Suggested Reading articles found!