Function and mechanism of cohesin REC8 during meiosis

doi:10.3785/j.issn.1008-9209.2022.08.121

Journal of Zhejiang University (Agriculture and Life Sciences)

2023, Vol. 49

Issue (5): 607-617 DOI: 10.3785/j.issn.1008-9209.2022.08.121

Young Scientist Forum

Function and mechanism of cohesin REC8 during meiosis

Jingling DAI(

),Chao YU

College of Life Sciences, Zhejiang University, Hangzhou 310058, Zhejiang, China

Download:

HTML

HTML ( )

PDF(2028KB)
Export: BibTeX | EndNote (RIS)

Abstract

Cohesin is a functionally and evolutionarily conserved multi-subunit protein complex that is required for sister chromatid cohesion and chromatin loop structure in both mitosis and meiosis. The meiotic cell-cycle consisting of one DNA replication and two successive rounds of chromosome segregation completes the segregation of homologous chromosomes and sister chromatids. Cohesin is crucial for faithful and proper segregations. There is a group of distinctive cohesin subunits that are only expressed in meiotic cells. The study of meiosis-specific cohesin is of great significance for understanding chromosome architecture and dynamics in meiosis. REC8 is a typical meiosis-specific cohesin subunit that plays essential roles in sister chromatid cohesion and meiotic chromosome events. Here, we review the function and mechanism of meiotic cohesin REC8 based on the current study and hypothesize that phosphorylation modification and microRNAs (miRNAs) could be the subsequent research directions of REC8.

Key words： meiosis cohesin REC8 cohesin cofactor chromosome homologous recombination

Received: 12 August 2022 Published: 03 November 2023

CLC:

Q71

Corresponding Authors: Chao YU E-mail: Jingling_dai@zju.edu.cn

	Service
	E-mail this article
	Add to my bookshelf
	Add to citation manager
	E-mail Alert
	RSS
	Articles by authors
	Jingling DAI
	Chao YU

Cite this article:

Jingling DAI,Chao YU. Function and mechanism of cohesin REC8 during meiosis. Journal of Zhejiang University (Agriculture and Life Sciences), 2023, 49(5): 607-617.

URL:

https://www.zjujournals.com/agr/10.3785/j.issn.1008-9209.2022.08.121 OR https://www.zjujournals.com/agr/Y2023/V49/I5/607

黏连蛋白REC8在减数分裂中的功能和机制

黏连蛋白（cohesin）是在功能和进化上高度保守的一类多亚基蛋白复合体，在细胞分裂过程中保障姐妹染色单体的黏连及染色质环结构的形成。减数分裂是一种特殊的细胞分裂方式，其经历1次DNA复制后连续进行2次细胞分裂，分别完成同源染色体与姐妹染色单体的分离，这一过程需要黏连蛋白的调控。在减数分裂中，存在1组不同于有丝分裂的特异型黏连蛋白。研究特异型黏连蛋白的功能和机制对于深入认识减数分裂过程中染色体结构与动力学行为具有重要意义。REC8是减数分裂特异型黏连蛋白复合体亚基之一，不但参与姐妹染色单体的黏合，还参与减数分裂染色体特异性事件的调控，对减数分裂的发生不可或缺。本文聚焦于减数分裂特异型黏连蛋白REC8，对其在减数分裂过程中的功能和作用机制进行综述，并从磷酸化修饰、微RNAs（microRNAs, miRNAs）等方面探讨了未来对REC8功能研究的方向。

关键词： 减数分裂, 黏连蛋白, REC8, 黏连蛋白辅因子, 染色体, 同源重组

Table 1 Components of cohesin complex in different species

Table 2 Key phenotypes observed in the mouse strains lacking for meiosis-specific cohesin coding gene

Fig. 1 Distribution of meiosis-specific cohesin complex on chromosomesA. REC8-type cohesin complex (REC8-SMC1β-SMC3-STAG3); B. RAD21L/RAD21-type cohesin complex (RAD21L/RAD21-SMC1α/β-SMC3-STAG3); C-D. REC8-type cohesin complex and RAD21L-type cohesin complex locate on chromosomes in a non-overlapping manner (REC8-type cohesin complex adheres to sister chromatids, while RAD21L-type cohesin complex adheres to non-sister chromatids of the homologous chromosomes); E. Location and dynamic change of REC8-type cohesin complex, RAD21L-type cohesin complex and RAD21-type cohesin complex during meiosis prophase Ⅰ.

Fig. 2 Synapsis associated with the location of cohesin complex in cohesin-mutant miceA. Homologous chromosome synapsis with closed-associated sister chromatids; B. Separated sister chromatid synapsis; C. Partial separated sister chromatid synapsis.

Fig. 3 Cleavage of REC8-type cohesin complex in a stepwise manner in meiosis mediated by cohesin cofactors


[1]	MEHTA G D, RIZVI S M, GHOSH S K. Cohesin: a guardian of genome integrity[J]. Biochimica et Biophysica Acta—Molecular Cell Research, 2012, 1823(8): 1324-1342. DOI: 10.1016/j.bbamcr.2012.05.027 doi: 10.1016/j.bbamcr.2012.05.027

[2]	ZHU Z, WANG X. Roles of cohesin in chromosome archi-tecture and gene expression[J]. Seminars in Cell and Develop-mental Biology, 2019, 90: 187-193. DOI: 10.1016/j.semcdb.2018.08.004 doi: 10.1016/j.semcdb.2018.08.004

[3]	ISHIGURO K I. The cohesin complex in mammalian meiosis[J]. Genes to Cells, 2019, 24(1): 6-30. DOI: 10.1111/gtc.12652 doi: 10.1111/gtc.12652

[4]	BISWAS U, HEMPEL K, LLANO E, et al. Distinct roles of meiosis-specific cohesin complexes in mammalian sperma-togenesis[J]. PLoS Genetics, 2016, 12(10): e1006389. DOI: 10.1371/journal.pgen.1006389 doi: 10.1371/journal.pgen.1006389

[5]	LEE J, HIRANO T. RAD21L, a novel cohesin subunit implicated in linking homologous chromosomes in mammalian meiosis[J]. Journal of Cell Biology, 2011, 192(2): 263-276. DOI: 10.1083/jcb.201008005 doi: 10.1083/jcb.201008005

[6]	FUKUDA T, FUKUDA N, AGOSTINHO A, et al. STAG3-mediated stabilization of REC8 cohesin complexes promotes chromosome synapsis during meiosis[J]. The EMBO Journal, 2014, 33(11): 1243-1255. DOI: 10.1002/embj.201387329 doi: 10.1002/embj.201387329

[7]	REVENKOVA E, EIJPE M, HEYTING C, et al. Novel meiosis-specific isoform of mammalian SMC1[J]. Molecular and Cellular Biology, 2001, 21(20): 6984-6998. DOI: 10.1128/MCB.21.20.6984-6998.2001 doi: 10.1128/MCB.21.20.6984-6998.2001

[8]	BISWAS U, STEVENSE M, JESSBERGER R. SMC1 alpha substitutes for many meiotic functions of SMC1 beta but cannot protect telomeres from damage[J]. Current Biology, 2018, 28(2): 249-261. DOI: 10.1016/j.cub.2017.12.020 doi: 10.1016/j.cub.2017.12.020

[9]	HERRÁN Y, GUTIÉRREZ-CABALLERO C, SÁNCHEZ-MARTÍN M, et al. The cohesin subunit RAD21L functions in meiotic synapsis and exhibits sexual dimorphism in fertility[J]. The EMBO Journal, 2011, 30(15): 3091-3105. DOI: 10.1038/emboj.2011.222 doi: 10.1038/emboj.2011.222

[10]	XU H, BEASLEY M D, WARREN W D, et al. Absence of mouse REC8 cohesin promotes synapsis of sister chromatids in meiosis[J]. Developmental Cell, 2005, 8(6): 949-961. DOI: 10.1016/j.devcel.2005.03.018 doi: 10.1016/j.devcel.2005.03.018

[11]	REVENKOVA E, EIJPE M, HEYTING C, et al. Cohesin SMC1 beta is required for meiotic chromosome dynamics, sister chromatid cohesion and DNA recombination[J]. Nature Cell Biology, 2004, 6(6): 555-562. DOI: 10.1038/ncb1135 doi: 10.1038/ncb1135

[12]	HOPKINS J, HWANG G, JACOB J, et al. Meiosis-specific cohesin component, Stag3 is essential for maintaining centromere chromatid cohesion, and required for DNA repair and synapsis between homologous chromosomes[J]. PLoS Genetics, 2014, 10(7): e1004413. DOI: 10.1371/journal.pgen.1004413 doi: 10.1371/journal.pgen.1004413

[13]	LLANO E, HERRAN Y, GARCIA-TUNON I, et al. Meiotic cohesin complexes are essential for the formation of the axial element in mice[J]. Journal of Cell Biology, 2012, 197(7): 877-885. DOI: 10.1083/jcb.201201100 doi: 10.1083/jcb.201201100

[14]	WARD A, HOPKINS J, MCKAY M, et al. Genetic inter-actions between the meiosis-specific cohesin components, STAG3, REC8, and RAD21L[J]. G3—Genes Genomes Genetics, 2016, 6(6): 1713-1724. DOI: 10.1534/g3.116.029462 doi: 10.1534/g3.116.029462

[15]	RONG M, MATSUDA A, HIRAOKA Y, et al. Meiotic cohesin subunits RAD21L and REC8 are positioned at distinct regions between lateral elements and transverse filaments in the synaptonemal complex of mouse sperma-tocytes[J]. Journal of Reproduction and Development, 2016, 62(6): 623-630. DOI: 10.1262/jrd.2016-127 doi: 10.1262/jrd.2016-127

[16]	ZHANG H, EMERSON D J, GILGENAST T G, et al. Chromatin structure dynamics during the mitosis-to-G1 phase transition[J]. Nature, 2019, 576(7785): 158-162. DOI: 10.1038/s41586-019-1778-y doi: 10.1038/s41586-019-1778-y

[17]	LI Y, HAARHUIS J, SEDENO C A, et al. The structural basis for cohesin-CTCF-anchored loops[J]. Nature, 2020, 578(7795): 472-476. DOI: 10.1038/s41586-019-1910-z doi: 10.1038/s41586-019-1910-z

[18]	DAVIDSON I F, BAUER B, GOETZ D, et al. DNA loop extrusion by human cohesin[J]. Science, 2019, 366(6471): 1338-1345. DOI: 10.1126/science.aaz3418 doi: 10.1126/science.aaz3418

[19]	BASTIE N, CHAPARD C, DAUBAN L, et al. Smc3 acetylation, Pds5 and Scc2 control the translocase activity that establishes cohesin-dependent chromatin loops[J]. Nature Structural and Molecular Biology, 2022, 29(6): 575-585. DOI: 10.1038/s41594-022-00780-0 doi: 10.1038/s41594-022-00780-0

[20]	HAARHUIS J, VAN DER WEIDE R H, BLOMEN V A, et al. The cohesin release factor WAPL restricts chromatin loop extension[J]. Cell, 2017, 169(4): 693-707. DOI: 10.1016/j.cell.2017.04.013 doi: 10.1016/j.cell.2017.04.013

[21]	SAKUNO T, TASHIRO S, TANIZAWA H, et al. Rec8 cohesin-mediated axis-loop chromatin architecture is required for meiotic recombination[J]. Nucleic Acids Research, 2022, 50(7): 3799-3816. DOI: 10.1093/nar/gkac183 doi: 10.1093/nar/gkac183

[22]	CHATZIDAKI E E, POWELL S, DEQUEKER B J H, et al. Ovulation suppression protects against chromosomal abnorma-lities in mouse eggs at advanced maternal age[J]. Current Biology, 2021, 31(18): 4038-4051. DOI: 10.1016/j.cub.2021.06.076 doi: 10.1016/j.cub.2021.06.076

[23]	TSUTSUMI M, FUJIWARA R, NISHIZAWA H, et al. Age-related decrease of meiotic cohesins in human oocytes[J]. PLoS ONE, 2014, 9(5): e96710. DOI: 10.1371/journal.pone.0096710 doi: 10.1371/journal.pone.0096710

[24]	UR S N, CORBETT K D. Architecture and dynamics of meiotic chromosomes[J]. Annual Review of Genetics, 2021, 55: 497-526. DOI: 10.1146/annurev-genet-071719-020235 doi: 10.1146/annurev-genet-071719-020235

[25]	BHATTACHARYYA T, WALKER M, POWERS N R, et al. Prdm9 and meiotic cohesin proteins cooperatively promote DNA double-strand break formation in mammalian sperma-tocytes[J]. Current Biology, 2019, 29(6): 1002-1018. DOI: 10.1016/j.cub.2019.02.007 doi: 10.1016/j.cub.2019.02.007

[26]	PASIERBEK P, JANTSCH M, MELCHER M, et al. A Caenorhabditis elegans cohesion protein with functions in meiotic chromosome pairing and disjunction[J]. Genes and Development, 2001, 15(11): 1349-1360. DOI: 10.1101/gad.192701 doi: 10.1101/gad.192701

[27]	SONG M H, ZHAI B Y, YANG X, et al. Interplay between Pds5 and Rec8 in regulating chromosome axis length and crossover frequency[J]. Science Advances, 2021, 7(11): eabe7920. DOI: 10.1126/sciadv.abe7920 doi: 10.1126/sciadv.abe7920

[28]	VIERA A, BERENGUER I, RUIZ-TORRES M, et al. PDS5 proteins regulate the length of axial elements and telomere integrity during male mouse meiosis[J]. EMBO Reports, 2020, 21(6): e49273. DOI: 10.15252/embr.201949273 doi: 10.15252/embr.201949273

[29]	CHEN Y Y, WANG Y, CHEN J, et al. The SUN1-SPDYA interaction plays an essential role in meiosis prophase I[J]. Nature Communications, 2021, 12: 3176. DOI: 10.1038/s41467-021-23550-w doi: 10.1038/s41467-021-23550-w

[30]	KLUTSTEIN M, FENNELL A, FERNANDEZ-ALVAREZ A, et al. The telomere bouquet regulates meiotic centromere assembly[J]. Nature Cell Biology, 2015, 17(4): 458-469. DOI: 10.1038/ncb3132 doi: 10.1038/ncb3132

[31]	HOU H, KYRIACOU E, THADANI R, et al. Centromeres are dismantled by foundational meiotic proteins Spo11 and Rec8[J]. Nature, 2021, 591(7851): 671-676. DOI: 10.1038/s41586-021-03279-8 doi: 10.1038/s41586-021-03279-8

[32]	GRAY S, COHEN P E. Control of meiotic crossovers: from double-strand break formation to designation[J]. Annual Review of Genetics, 2016, 50: 175-210. DOI: 10.1146/annurev-genet-120215-035111 doi: 10.1146/annurev-genet-120215-035111

[33]	PHIPPS J, DUBRANA K. DNA repair in space and time: safeguarding the genome with the cohesin complex[J]. Genes, 2022, 13(2): 198. DOI: 10.3390/genes13020198 doi: 10.3390/genes13020198

[34]	KUMAR R, OLIVER C, BRUN C, et al. Mouse REC114 is essential for meiotic DNA double-strand break formation and forms a complex with MEI4[J]. Life Science Alliance, 2018, 1(6): e201800259. DOI: 10.26508/lsa.201800259 doi: 10.26508/lsa.201800259

[35]	ROBERT T, NORE A, BRUN C, et al. The TopoVIB-like protein family is required for meiotic DNA double-strand break formation[J]. Science, 2016, 351(6276): 943-949. DOI: 10.1126/science.aad5309 doi: 10.1126/science.aad5309

[36]	POWERS N R, PARVANOV E D, BAKER C L, et al. The meiotic recombination activator PRDM9 trimethylates both H3K36 and H3K4 at recombination hotspots in vivo [J]. PLoS Genetics, 2016, 12(6): e1006146. DOI: 10.1371/journal.pgen.1006146 doi: 10.1371/journal.pgen.1006146

[37]	TIAN H, BILLINGS T, PETKOV P M. EWSR1 affects PRDM9-dependent histone 3 methylation and provides a link between recombination hotspots and the chromosome axis protein REC8[J]. Molecular Biology of the Cell, 2021, 32(1): 1-14. DOI: 10.1091/mbc.E20-09-0604 doi: 10.1091/mbc.E20-09-0604

[38]	KLEIN F, MAHR P, GALOVA M, et al. A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis[J]. Cell, 1999, 98(1): 91-103. DOI: 10.1016/S0092-8674(00)80609-1 doi: 10.1016/S0092-8674(00)80609-1

[39]	WANG S, ZICKLER D, KLECKNER N, et al. Meiotic crossover patterns: obligatory crossover, interference and homeostasis in a single process[J]. Cell Cycle, 2015, 14(3): 305-314. DOI: 10.4161/15384101.2014.991185 doi: 10.4161/15384101.2014.991185

[40]	WANG Y, ZHAI B Y, TAN T C, et al. ESA1 regulates meiotic chromosome axis and crossover frequency via acetylating histone H4[J]. Nucleic Acids Research, 2021, 49(16): 9353-9373. DOI: 10.1093/nar/gkab722 doi: 10.1093/nar/gkab722

[41]	YOON S W, LEE M S, XAVER M, et al. Meiotic prophase roles of Rec8 in crossover recombination and chromosome structure[J]. Nucleic Acids Research, 2016, 44(19): 9296-9314. DOI: 10.1093/nar/gkw682 doi: 10.1093/nar/gkw682

[42]	DING D Q, MATSUDA A, OKAMASA K, et al. Meiotic cohesin-based chromosome structure is essential for homologous chromosome pairing in Schizosaccharomyces pombe [J]. Chromosoma, 2016, 125(2): 205-214. DOI: 10.1007/s00412-015-0551-8 doi: 10.1007/s00412-015-0551-8

[43]	ISHIGURO K, KIM J, SHIBUYA H, et al. Meiosis-specific cohesin mediates homolog recognition in mouse sperma-tocytes[J]. Genes and Development, 2014, 28(6): 594-607. DOI: 10.1101/gad.237313.113 doi: 10.1101/gad.237313.113

[44]	AGOSTINHO A, MANNEBERG O, VAN SCHENDEL R, et al. High density of REC8 constrains sister chromatid axes and prevents illegitimate synaptonemal complex formation[J]. EMBO Reports, 2016, 17(6): 901-913. DOI: 10.15252/embr.201642030 doi: 10.15252/embr.201642030

[45]	ISHIGURO K, WATANABE Y. The cohesin REC8 prevents illegitimate inter-sister synaptonemal complex assembly[J]. EMBO Reports, 2016, 17(6): 783-784. DOI: 10.15252/embr.201642544 doi: 10.15252/embr.201642544

[46]	VISNES T, GIORDANO F, KUZNETSOVA A, et al. Localisation of the SMC loading complex Nipbl/Mau2 during mammalian meiotic prophase Ⅰ[J]. Chromosoma, 2014, 123(3): 239-252. DOI: 10.1007/s00412-013-0444-7 doi: 10.1007/s00412-013-0444-7

[47]	BOAVIDA A, SANTOS D, MAHTAB M, et al. Functional coupling between DNA replication and sister chromatid cohesion establishment[J]. International Journal of Molecular Sciences, 2021, 22(6): 2810. DOI: 10.3390/ijms22062810 doi: 10.3390/ijms22062810

[48]	ALOMER R M, DA S E, CHEN J, et al. Esco1 and Esco2 regulate distinct cohesin functions during cell cycle progre-ssion[J]. PNAS, 2017, 114(37): 9906-9911. DOI: 10.1073/pnas.1708291114 doi: 10.1073/pnas.1708291114

[49]	NISHIYAMA T, LADURNER R, SCHMITZ J, et al. Sororin mediates sister chromatid cohesion by antagonizing Wapl[J]. Cell, 2010, 143(5): 737-749. DOI: 10.1016/j.cell.2010.10.031 doi: 10.1016/j.cell.2010.10.031

[50]	NISHIYAMA T, SYKORA M M, HUIS I T V P, et al. Aurora B and Cdk1 mediate Wapl activation and release of acetylated cohesin from chromosomes by phosphorylating Sororin[J]. PNAS, 2013, 110(33): 13404-13409. DOI: 10.1073/pnas.1305020110 doi: 10.1073/pnas.1305020110

[51]	BRIENO-ENRIQUEZ M A, MOAK S L, TOLEDO M, et al. Cohesin removal along the chromosome arms during the first meiotic division depends on a NEK1-PP1 gamma-WAPL axis in the mouse[J]. Cell Reports, 2016, 17(4): 977-986. DOI: 10.1016/j.celrep.2016.09.059 doi: 10.1016/j.celrep.2016.09.059

[52]	CHALLA K, SHINOHARA M, SHINOHARA A. Meiotic prophase-like pathway for cleavage-independent removal of cohesin for chromosome morphogenesis[J]. Current Genetics, 2019, 65(4): 817-827. DOI: 10.1007/s00294-019-00959-x doi: 10.1007/s00294-019-00959-x

[53]	CHALLA K, FAJISH V G, SHINOHARA M, et al. Meiosis-specific prophase-like pathway controls cleavage-independent release of cohesin by Wapl phosphorylation[J]. PLoS Genetics, 2019, 15(1): e1007851. DOI: 10.1371/journal.pgen.1007851 doi: 10.1371/journal.pgen.1007851

[54]	KATIS V L, LIPP J J, IMRE R, et al. Rec8 phosphorylation by casein kinase 1 and Cdc7-Dbf4 kinase regulates cohesin cleavage by separase during meiosis[J]. Developmental Cell, 2010, 18(3): 397-409. DOI: 10.1016/j.devcel.2010.01.014 doi: 10.1016/j.devcel.2010.01.014

[55]	FERRANDIZ N, BARROSO C, TELECAN O, et al. Spatio-temporal regulation of Aurora B recruitment ensures release of cohesion during C. elegans oocyte meiosis[J]. Nature Communications, 2018, 9: 834. DOI: 10.1038/s41467-018-03229-5 doi: 10.1038/s41467-018-03229-5

[56]	NIKALAYEVICH E, EL J S, DUPRE A, et al. Aurora B/C-dependent phosphorylation promotes Rec8 cleavage in mammalian oocytes[J]. Current Biology, 2022, 32(10): 2281-2290. DOI: 10.1016/j.cub.2022.03.041 doi: 10.1016/j.cub.2022.03.041

[57]	KUDO N R, ANGER M, PETERS A H, et al. Role of cleavage by separase of the Rec8 kleisin subunit of cohesin during mammalian meiosis Ⅰ[J]. Journal of Cell Science, 2009, 122(Pt 15): 2686-2698. DOI: 10.1242/jcs.035287 doi: 10.1242/jcs.035287

[58]	EL Y W, BUFFIN E, CLADIERE D, et al. Mps1 kinase-dependent Sgo2 centromere localisation mediates cohesin protection in mouse oocyte meiosis Ⅰ[J]. Nature Communi-cations, 2017, 8: 694. DOI: 10.1038/s41467-017-00774-3 doi: 10.1038/s41467-017-00774-3

[59]	ZHANG Y L, ZHANG H, GAO Y J, et al. Protein phos-phatase 2A b ´ α and b ´ β protect centromeric cohesion during meiosis Ⅰ[J]. Plant Physiology, 2019, 179(4): 1556-1568. DOI: 10.1104/pp.18.01320 doi: 10.1104/pp.18.01320

[60]	MA W, ZHOU J W, CHEN J, et al. Meikin synergizes with shugoshin to protect cohesin Rec8 during meiosis Ⅰ[J]. Genes and Development, 2021, 35(9/10): 692-697. DOI: 10.1101/gad.348052.120 doi: 10.1101/gad.348052.120

[61]	CHAMBON J P, TOUATI S A, BERNEAU S, et al. The PP2A inhibitor I2PP2A is essential for sister chromatid segregation in oocyte meiosis Ⅱ[J]. Current Biology, 2013, 23(6): 485-490. DOI: 10.1016/j.cub.2013.02.004 doi: 10.1016/j.cub.2013.02.004

[62]	JONAK K, ZAGORIY I, OZ T, et al. APC/CCdc20 mediates deprotection of centromeric cohesin at meiosis Ⅱ in yeast[J]. Cell Cycle, 2017, 16(12): 1145-1152. DOI: 10.1080/15384101.2017.1320628 doi: 10.1080/15384101.2017.1320628

[63]	CHEN J, GAO C X, LUO M C, et al. MicroRNA-202 safeguards meiotic progression by preventing premature SEPARASE-mediated REC8 cleavage[J]. EMBO Reports, 2022, 23(8): e54298. DOI: 10.15252/embr.202154298 doi: 10.15252/embr.202154298

[64]	TUCKER E J, BELL K M, ROBEVSKA G, et al. Meiotic genes in premature ovarian insufficiency: variants in HROB and REC8 as likely genetic causes[J]. European Journal of Human Genetics, 2022, 30(2): 219-228. DOI: 10.1038/s41431-021-00977-9 doi: 10.1038/s41431-021-00977-9

[1]	XIA Xue, GU Jinhua, LIU Dan, WU Yimei, TIAN Yuxiao, CHEN Qing, ZHANG Fen, TANG Haoru, SUN Bo. Optimization of chromosome preparation and karyotype analysis of yellow-flower Chinese kale[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2016, 42(5): 527-.

[2]	Zhang Jianhui, Wang Shoufeng. Expression of Astragalus membranaceus phenylalanine ammonia-lyase gene in Pichia pastoris*[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2014, 40(1): 1-8.

Viewed

Full text

Abstract

Cited

Shared

Discussed