Welcome to Acta Agronomica Sinica，

Acta Agronomica Sinica ›› 2023, Vol. 49 ›› Issue (9): 2344-2361.doi: 10.3724/SP.J.1006.2023.24246

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

Relative expression patterns of laccase gene family members in upland Gossypium hirsutum L.

ZUO Chun-Yang(), LI Ya-Wei, LI Yan-Long, JIN Shuang-Xia, ZHU Long-Fu, ZHANG Xian-Long, MIN Ling()   

  1. National Key Laboratory of Crop Genetic Improvement / Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan 430070, Hubei, China
  • Received:2022-11-02 Accepted:2023-02-21 Online:2023-09-12 Published:2023-03-13
  • About author:First author contact:**Contributed equally to this work
  • Supported by:
    Major Project of Hubei Hongshan Laboratory(2022hszd004);National Natural Science Foundation of China “Regulatory Network Analysis of GhHRK Gene Enhancing Pollen High Temperature Tolerance in Cotton”(32072024)

RichHTML414

45

PDF

255

Abstract:

Laccase, a member of the blue copper oxidase protein family, plays an important role in plant lignin synthesis and improving plant resistance to stress. In this study, 104 members of the Laccase gene (GhLAC) family were identified from the upland cotton genome. Phylogenetic tree and tissue expression map were constructed. Twenty genes were randomly selected for qRT-PCR analysis to verify the results of expression heat map. To further explore the role of laccase in cotton, promoter-GUS fusion vectors were transformed into Arabidopsis thaliana. The detailed expression patterns of six members of the Laccase gene family (GhLAC12A, GhLAC14A, GhLAC20A, GhLAC25D, GhLAC59D, and GhLAC63D) were studied by GUS staining in different tissues during different developmental period of transgenic Arabidopsis thaliana. To explore the role of laccase in stress, the expression of the six laccase genes was analyzed by cutting and piercing, and the corresponding genes were analyzed by qRT-PCR using the anther of two cotton strains ‘84021’ (high temperature tolerant) and ‘H05’ (high temperature sensitive) at different stages under normal and high temperature conditions. The results showed that 20 randomly selected genes were differentially expressed in six tissues of root, stem, leaf, petal, anther, and stigma, and the relative expression levels of most genes were consistent with the transcriptome data. The promoter of six laccase genes could drive GUS gene expression in different levels at germination, two-leaf, and four-leaf stages. The trauma treatment indicated that the promoter of GhLAC12A and GhLAC14A significantly improved the ability to drive GUS protein expression in leaves after trauma induction, suggesting that the two genes might be involved in traumatic stress response. In addition, the relative expression levels of the six GhLACs genes were significantly down-regulated after high temperature stress at the tetrad stage and anther dehiscence stage of cotton strain ‘84021’, suggesting GhLACs gene might negatively regulate the high temperature tolerance of cotton anthers. The results of this study provide the reference for further exploring the function of laccase family genes.

Key words: Gossypium hirsutum L., laccase gene, the promoter-GUS expression pattern, anther response to high temperature, wound induced expression

Table 1

Sequence and purpose of the primers used in this study"

引物名称 Primer name 引物序列 Prime sequence (5°-3°) 用途 Purpose
ubiquitin7-F GAAGGCATTCCACCTGACCAAC 实时荧光定量PCR
ubiquitin7-R CTTGACCTTCTTCTTCTTGTGCTTG qRT-PCR
GhLAC1A-F AATGGCAACAACTTCACATC 实时荧光定量PCR
GhLAC1A-R ACACTCAGAATGGTCCTCGT qRT-PCR
GhLAC12A-F GCTAATCAAACCATTGCTCCTG 实时荧光定量PCR
GhLAC12A-R TCCGACAATCGTCAATCTGTG qRT-PCR
GhLAC14A-F CCTATTGAGGAAGGGACGAG 实时荧光定量PCR
GhLAC14A-R ACCATACTCCGGGATTGGTA qRT-PCR
GhLAC20A-F CCAACTTCTTCGTAGTCGGTAG 实时荧光定量PCR
GhLAC20A-R ATCCCTGGGTTATCTGCTCT qRT-PCR
GhLAC31A-F CCAAGGCGAAACGAATCTTA 实时荧光定量PCR
GhLAC31A-R ATTAGGGCCACCTCCTGTCT qRT-PCR
GhLAC36A-F TGCCAAGAGCATCGTAACCG 实时荧光定量PCR
GhLAC36A-R TCCGTCCGCCCATCCAGTTC qRT-PCR
GhLAC38A-F AGATTCGGGTCCGCAGAGGG 实时荧光定量PCR
GhLAC38A-R CAGCCCAAGCACTGGTAGCG qRT-PCR
GhLAC40A-F GGGTTCTATTTCTAAGCACTTT 实时荧光定量PCR
GhLAC40A-R ACTATCGTTTACGACCAGCA qRT-PCR
GhLAC43A-F AAGAAGGAACATTGTGGTGGCA 实时荧光定量PCR
GhLAC43A-R CCCGGAGTCGATGGGAACTA qRT-PCR
GhLAC6D-F CCAGTTAAACCAGGGAAGAC 实时荧光定量PCR
GhLAC6D-R AGAGCCGGAGTAATGTAAGG qRT-PCR
GhLAC11D-F CCTTAATCCACCAGTATTCTACG 实时荧光定量PCR
GhLAC11D-R AGTTTAGCACAACAGCCCTC qRT-PCR
GhLAC23D-F ACCATTCACTGGCACGGTGTT 实时荧光定量PCR
GhLAC23D-R ACGGATACGATTCATTACGC qRT-PCR
GhLAC25D-F CAATTCCCTGCCTTAGTCCC 实时荧光定量PCR
GhLAC25D-R TTGTCCCAGTCATCGTTTGC qRT-PCR
GhLAC28D-F GGCAGTTACGGTTATCTTGT 实时荧光定量PCR
GhLAC28D-R TTGGGAGGATGATGAGTGGG qRT-PCR
GhLAC54D-F GGGTGTTATCATCTATCAGGG 实时荧光定量PCR
GhLAC54D-R ACATTAAGTGGGACAGGGAC qRT-PCR
GhLAC57D-F TCTCCTGGACAGACCATAGA 实时荧光定量PCR
GhLAC57D-R AGTAGAATAAGCCCTAGCAAC qRT-PCR
GhLAC58D-F TGAGACAGACCCAAGCACAT 实时荧光定量PCR
GhLAC58D-R GACAACGAGGCATGGTAGAT qRT-PCR
GhLAC59D-F ATTGGCAAGGGTTTGAGGAT 实时荧光定量PCR
GhLAC59D-R ACGTAGGTGTAGGGAAAGGATA qRT-PCR
GhLAC61D-F TTGAATGCGATCTGGCTGTT 实时荧光定量PCR
GhLAC61D-R ATGGTGGTCATGGTAGTTGGAATA qRT-PCR
GhLAC63D-F ACTTCCGTGCTCATGTTAGG 实时荧光定量PCR
GhLAC63D-R CAAGAGGCAGACTTGTATTCG qRT-PCR

Fig. 1

Phylogenic tree of LACs gene family in Arabidopsis, rice, and Gossypium hirsutum L."

Table 2

Information of LAC gene family in Gossypium hirsutum L."

基因ID
Gene ID		 染色体
Chr.		 基因描述(拟南芥)
Gene description (Arabidopsis)		 基因组位置 Genomic position 命名
Name
起始 Start 终止 End
Ghir_A01G021510 A01 Laccase-17 116737831 116742782 GhLAC1A
Ghir_D01G023050 D01 Laccase-17 62359392 62363270 GhLAC1D
Ghir_A01G021950 A01 Laccase-4 117127088 117132069 GhLAC2A
Ghir_D01G023480 D01 Laccase-4 62708521 62717375 GhLAC2D
Ghir_A02G006480 A02 Laccase-21 10086940 10089681 GhLAC3A
Ghir_D02G006860 D02 Laccase-21 9508400 9511507 GhLAC3D
Ghir_A03G005270 A03 Laccase-2 9138986 9141467 GhLAC4A
Ghir_D03G013500 D03 Laccase-2 44314668 44316870 GhLAC4D
Ghir_A03G005280 A03 Laccase-2 9197235 9204292 GhLAC5A
Ghir_D03G013490 D03 Laccase-2 44287872 44290796 GhLAC5D
Ghir_A03G005800 A03 Laccase-4 10413905 10417019 GhLAC6A
Ghir_D03G013060 D03 Laccase-4 43363895 43367056 GhLAC6D
Ghir_A04G009430 A04 Laccase-7 71412678 71434702 GhLAC7A
Ghir_D04G013660 D04 Laccase-7 45073981 45077137 GhLAC7D
Ghir_A04G009470 A04 Laccase-7 71627753 71631136 GhLAC8A
Ghir_D04G013680 D04 Laccase-7 45181487 45184916 GhLAC8D
Ghir_A05G009230 A05 Laccase-4 8476727 8479903 GhLAC9A
Ghir_D05G009240 D05 Laccase-4 7540512 7543586 GhLAC9D
Ghir_A05G010150 A05 Laccase-17 9143475 9146068 GhLAC10A
Ghir_D05G009870 D05 Laccase-17 8212961 8215461 GhLAC10D
Ghir_A05G025140 A05 Laccase-15 25644784 25662157 GhLAC11A
Ghir_D05G025180 D05 Laccase-14 23486473 23489452 GhLAC11D
Ghir_A05G025310 A05 Laccase-14 25939177 25941026 GhLAC12A
Ghir_D05G025230 D05 Laccase-14 23586804 23588738 GhLAC12D
Ghir_A05G025330 A05 Laccase-14 25973262 25976026 GhLAC13A
Ghir_D05G025210 D05 Laccase-14 23560592 23563227 GhLAC13D
Ghir_A05G025340 A05 Laccase-14 25981068 25989683 GhLAC14A
Ghir_D05G025200 D05 Laccase-14 23542194 23557617 GhLAC14D
Ghir_A05G025350 A05 Putative laccase-9 26015294 26017921 GhLAC15A
Ghir_D05G025190 D05 Putative laccase-9 23514531 23517069 GhLAC15D
Ghir_A05G031190 A05 Laccase-22 41692291 41698066 GhLAC16A
Ghir_D05G031070 D05 Laccase-22 33904186 33908534 GhLAC16D
Ghir_A06G012170 A06 Putative laccase-9 67269136 67271306 GhLAC17A
Ghir_D06G012330 D06 Putative laccase-9 29988284 29990547 GhLAC17D
Ghir_A08G021230 A08 Laccase-3 116971139 116973684 GhLAC18A
Ghir_D08G022010 D08 Laccase-3 63494311 63496810 GhLAC18D
Ghir_A09G016340 A09 Laccase-17 72475738 72478310 GhLAC19A
Ghir_D09G015810 D09 Laccase-17 44179260 44181960 GhLAC19D
Ghir_A10G023410 A10 Laccase-22 112560879 112563710 GhLAC20A
Ghir_D10G025960 D10 Laccase-22 66026294 66029136 GhLAC20D
Ghir_A10G024200 A10 Laccase-5 114093313 114095981 GhLAC21A
Ghir_D10G026620 D10 Laccase-5 67161382 67164003 GhLAC21D
Ghir_A11G019640 A11 Laccase-6 27309104 27311987 GhLAC22A
Ghir_D11G019420 D11 Laccase-11 21681414 21682836 GhLAC22D
Ghir_A11G035330 A11 Laccase-17 122965170 122967669 GhLAC23A
Ghir_D11G036190 D11 Laccase-17 72693575 72696286 GhLAC23D
Ghir_A11G035350 A11 Laccase-4 122971778 122974013 GhLAC24A
Ghir_D11G036210 D11 Laccase-17 72700213 72702426 GhLAC24D
Ghir_A11G035490 A11 Laccase-4 123045551 123048240 GhLAC25A
Ghir_D11G036340 D11 Laccase-4 72775350 72777973 GhLAC25D
Ghir_A13G001780 A13 Laccase-17 2014792 2017130 GhLAC26A
Ghir_D13G002060 D13 Laccase-17 1759037 1761649 GhLAC26D
Ghir_A13G002160 A13 Laccase-17 2565151 2567561 GhLAC27A
Ghir_D13G002440 D13 Laccase-17 2206264 2213052 GhLAC27D
Ghir_A13G002170 A13 Laccase-17 2580835 2585183 GhLAC28A
Ghir_D13G024730 D13 Laccase-2 62656628 62661237 GhLAC28D
Ghir_A13G002350 A13 Laccase-11 2736016 2738294 GhLAC29A
Ghir_D13G002640 D13 Laccase-11 2386833 2389243 GhLAC29D
Ghir_A13G023990 A13 Laccase-2 107564582 107569198 GhLAC30A
Ghir_D11G010590 D11 Laccase-6 9024231 9027561 GhLAC30D
Ghir_A03G005300 A03 Laccase-2 9235739 9242786 GhLAC31A
Ghir_A03G007710 A03 Laccase-11 17682089 17684169 GhLAC32A
Ghir_A04G009070 A04 Laccase-17 69641501 69641989 GhLAC33A
Ghir_A04G009440 A04 Laccase-9 71412678 71415616 GhLAC34A
Ghir_A04G009460 A04 Laccase-7 71525265 71528510 GhLAC35A
Ghir_A05G010190 A05 Laccase-17 9194020 9196191 GhLAC36A
Ghir_A05G025150 A05 Laccase-14 25668096 25669929 GhLAC37A
Ghir_A05G025280 A05 Laccase-14 25869242 25871007 GhLAC38A
Ghir_A05G025290 A05 Laccase-14 25890847 25893461 GhLAC39A
Ghir_A05G025320 A05 Laccase-14 25951588 25954197 GhLAC40A
Ghir_A05G031330 A05 Laccase-12 42716069 42718551 GhLAC41A
Ghir_A06G017280 A06 Laccase-5 116079600 116081862 GhLAC42A
Ghir_A06G017290 A06 Laccase-5 116189142 116197901 GhLAC43A
Ghir_A06G017300 A06 Laccase-5 116223123 116225599 GhLAC44A
Ghir_A06G017320 A06 Laccase-5 116280847 116285027 GhLAC45A
Ghir_A10G009410 A10 Laccase-11 18971904 18974558 GhLAC46A
Ghir_A11G010610 A11 Laccase-6 9769950 9772299 GhLAC47A
Ghir_A12G012190 A12 Laccase-6 80351644 80353970 GhLAC48A
Ghir_A13G003100 A13 Laccase-11 3705196 3707259 GhLAC49A
Ghir_A13G003110 A13 Laccase-11 3713263 3720273 GhLAC50A
Ghir_D03G010220 D03 Laccase-11 35974903 35978183 GhLAC51D
Ghir_D03G013470 D03 Laccase-17 44265628 44266723 GhLAC52D
Ghir_D03G015740 D03 Laccase-3 48218625 48221114 GhLAC53D
Ghir_D04G013650 D04 Laccase-9 44922823 44925840 GhLAC54D
Ghir_D04G013670 D04 Laccase-7 45158044 45161359 GhLAC55D
Ghir_D04G013870 D04 Laccase-4 45597220 45599865 GhLAC56D
Ghir_D05G025170 D05 Laccase-15 23475679 23484348 GhLAC57D
Ghir_D05G025220 D05 Putative laccase-9 23575706 23578427 GhLAC58D
Ghir_D05G027760 D05 Laccase-14 26649634 26651370 GhLAC59D
Ghir_D05G031170 D05 Laccase-12 34446602 34448100 GhLAC60D
Ghir_D05G031210 D05 Laccase-22 34596389 34597068 GhLAC61D
Ghir_D06G018210 D06 Laccase-5 59288750 59291253 GhLAC62D
Ghir_D06G018220 D06 Laccase-5 59357081 59359262 GhLAC63D
Ghir_D06G018230 D06 Laccase-5 59458411 59459122 GhLAC64D
Ghir_D06G018250 D06 Laccase-5 59500342 59502844 GhLAC65D
Ghir_D10G009840 D10 Laccase-11 11987141 11989232 GhLAC66D
Ghir_D10G014410 D10 Laccase-2 25717367 25718684 GhLAC67D
Ghir_D11G019730 D11 Laccase-6 22309695 22312399 GhLAC68D
Ghir_D12G012430 D12 Laccase-6 41466012 41468206 GhLAC69D
Ghir_D13G003370 D13 Laccase-11 3233418 3235743 GhLAC70D
Ghir_D13G003390 D13 Laccase-11 3256191 3258374 GhLAC71D
Ghir_D13G009820 D13 Laccase-8 22859921 22864788 GhLAC72D
Ghir_A08G026500 Scaffold2204 Laccase-7 49182 53499 GhLAC73
Ghir_A03G023780 Scaffold2615 Laccase-3 13682 16169 GhLAC74

Fig. 2

Relative expression pattern of GhLAC genes based on transcriptome data A: heat map of GhLAC gene family expression in root, stem, leaf, petal, anther, and stigma of H05. B: the classification of highly expressed genes in different tissues."

Fig. 3

Tissue expression analysis of some members of LAC gene family in Gossypium hirsutum L. R: root; S: stem; L: leaf; P: petal; St: stigma; A: anther. The error value represents the standard deviation of the three replicates, and GhUBQ7 (Gh_A11G011460) was the internal reference gene. Different letters indicate significantly different at P < 0.05 by one-way ANOVA."

Fig. 4

Detection of GUS gene expression driven by the promoter of six GhLACs at seed germination stage Stage 1: the early seed germination stage; Stage 2: the later seed germination stage. RH: root hair; Ra: radicle. Bar: 200 μm."

Fig. 5

Detection of GUS gene expression driven by the promoter of six GhLAC genes at two-leaf stage and four-leaf stages Stage 1: two-leaf stage; Stage 2: four-leaf stage. Tr: trichome. Bar: 1 mm. (A-F) and (G-L): the relative expression pattern of ProGhLAC12A, ProGhLAC14A, ProGhLAC20A, ProGhLAC25D, ProGhLAC59D, and ProGhLAC63D at two-leaf (A-F) and four-leaf (G-L) stages; (M-R) and (S-X): the analysis of leaf (M-R) and root (S-X) expression patterns of ProGhLAC12A, ProGhLAC14A, ProGhLAC20A, ProGhLAC25D, ProGhLAC59D, and ProGhLAC63D at four-leaf stage."

Fig. 6

GUS gene expression analysis driven by the promoter of six GhLAC genes in inflorescence and leaves of mature plants (A-F) and (G-L) represent the expression of GUS gene driven by the promoter of GhLAC12A, GhLAC14A, GhLAC20A, GhLAC25D, GhLAC59D, and GhLAC63D genes in flowering and leave at mature stage, respectively. An: anther. Bar: 1 mm."

Fig. 7

Expression patterns induced by trauma at the two leaf stage and four leaf stages A and B: the expression patterns induced by trauma at the two leaf seedling stage (A) and four leaf seedling stage (B). CK: the control group; C: cutting group; P: piercing group. The red arrow represents cutting treatment, and the white arrow represents piercing treatment. Bar: 2 mm."

Fig. 8

Relative expression pattern of six GhLAC genes under high temperature The relative expression pattern of GhLAC genes was performed in 84021 (high temperature tolerance line) and H05 (high temperature sensitive line) anthers at TS (tetrad stage; 6- to 7-mm bud), TDS (tapetal degradation stage; 9-14 mm bud), and ADS (anther dehiscence stage; more than 24-mm bud) under NT and HT by qRT-PCR. HN: H05 under normal temperature; HH: H05 under high temperature; 8N: 84021 under normal temperature; 8H: 84021 under high temperature. The error value represents the standard deviation of three biological replicates, and GhUBQ7 (Gh_A11G011460) as the internal reference gene. Asterisks indicate significant differences (* P < 0.05, ** P < 0.01) by Student’s t-test."

[1] Hüttermann A, Mai C, Kharazipour A. Modification of lignin for the production of new compounded materials. Appl Microbiol Biot, 2001, 55: 387-394.
doi: 10.1007/s002530000590
[2] Piontek K, Antorini M, Choinowski T. Crystal structure of a laccase from the fungus Trametes versicolor at 1.90-A resolution containing a full complement of coppers. J Biol Chem, 2002, 277: 37663-37669.
doi: 10.1074/jbc.M204571200 pmid: 12163489
[3] Claus H. Laccases: structure, reactions, distribution. Micron, 2004, 35: 93-96.
doi: 10.1016/j.micron.2003.10.029 pmid: 15036303
[4] Ander P, Eriksson K E. The importance of phenol oxidase activity in lignin degradation by the white rot fungus Sporotrichum pulverulentum. Arch Microbiol, 1976, 109: 1-8.
doi: 10.1007/BF00425105
[5] Williamson P R. Laccase and melanin in the pathogenesis of Cryptococcus neoformans. Front Biosci, 1997, 2: 99-107.
[6] Carbajo J M, Junca H, Terrón M C, González T, Yagüe S, Zapico E, González A E. Tannic acid induces transcription of laccase gene cglcc1 in the white-rot fungus Coriolopsis gallica. Can J Microbiol, 2002, 48: 1041-1047.
pmid: 12619815
[7] Weech M H, Chapleau M, Pan L, Ide C, Bede J C. Caterpillar saliva interferes with induced Arabidopsis thaliana defence responses via the systemic acquired resistance pathway. J Exp Bot, 2008, 59: 2437-2448.
doi: 10.1093/jxb/ern108
[8] Sterjiades R, Dean J F D, Eriksson K E. Laccase from sycamore maple (Acer pseudoplatanus) polymerizes monolignols. Plant Physiol, 1992, 99: 1162-1168.
doi: 10.1104/pp.99.3.1162 pmid: 16668984
[9] Liang M, Davis E, Gardner D, Cai X, Wu Y. Involvement of AtLAC15 in lignin synthesis in seeds and in root elongation of Arabidopsis. Planta, 2006, 224: 1185-1196.
doi: 10.1007/s00425-006-0300-6
[10] Wang G D, Li Q J, Luo B, Chen X Y. Ex planta phytoremediation of trichlorophenol and phenolic allelochemicals via an engineered secretory laccase. Nat Biotechnol, 2004, 22: 893-897.
doi: 10.1038/nbt982
[11] Bao W, O’Malley D M, Whetten R, Sederoff R R. A laccase associated with lignification in loblolly pine xylem. Science, 1993, 260: 672-674.
pmid: 17812228
[12] Berthet S, Demont C N, Pollet B, Bidzinski P, Cézard L, Le B P, Borrega N, Hervé J, Blondet E, Balzergue S, Lapierre C, Jouanin L. Disruption of LACCASE4 and 17 results in tissue-specific alterations to lignification of Arabidopsis thaliana stems. Plant Cell, 2011, 23: 1124-1137.
doi: 10.1105/tpc.110.082792
[13] Miguel P A, Schneider I, Kroll P, Hofhuis H, Metzger S, Pauly M, Hay A. Explosive seed dispersal depends on SPL7 to ensure sufficient copper for localized lignin deposition via laccases. Proc Natl Acad Sci USA, 2022, 119: e2202287119.
[14] Zhang Y C, Yu Y, Wang C Y, Li Z Y, Liu Q, Xu J, Liao J Y, Wang X J, Qu L H, Chen F, Xin P, Yan C, Chu J, Li H Q, Chen Y Q. Overexpression of microRNA OsmiR397 improves rice yield by increasing grain size and promoting panicle branching. Nat Biotechnol, 2013, 31: 848-852.
doi: 10.1038/nbt.2646 pmid: 23873084
[15] Zhong J, He W J, Peng Z, Zhang H, Li F, Yao J L. A putative AGO protein, OsAGO17, positively regulates grain size and grain weight through OsmiR397b in rice. Plant Biotechnol J, 2020, 18: 916-928.
doi: 10.1111/pbi.13256 pmid: 31529568
[16] Sun Y J, Xiong X G, Wang Q, Zhu L, Wang L, He Y, Zeng H L. Integrated analysis of small RNA, transcriptome, and degradome sequencing reveals the miR156, miR5488 and miR399 are involved in the regulation of male sterility in PTGMS rice. Int J Mol Sci, 2021, 22: 2260.
doi: 10.3390/ijms22052260
[17] Mayer A M, Staples R C. Laccase: new functions for an old enzyme. Phytochemistry, 2002, 60: 551-565.
doi: 10.1016/s0031-9422(02)00171-1 pmid: 12126701
[18] Jiao X Y, Li G Q, Wang Y, Nie F, Cheng X, Abdullah M, Lin Y, Cai Y P. Systematic analysis of the pleurotus ostreatus laccase gene (PoLac) family and functional characterization of PoLac2 involved in the degradation of cotton-straw lignin. Molecules, 2018, 23: 880.
doi: 10.3390/molecules23040880
[19] Li L, Steffens J C. Overexpression of polyphenol oxidase in transgenic tomato plants results in enhanced bacterial disease resistance. Planta, 2002, 215: 239-247.
doi: 10.1007/s00425-002-0750-4 pmid: 12029473
[20] Choi G H, Larson T G, Nuss D L. Molecular analysis of the laccase gene from the chestnut blight fungus and selective suppression of its expression in an isogenic hypovirulent strain. Mol Plant Microbe Interact, 1992, 5: 119-128.
doi: 10.1094/MPMI-5-119
[21] Zhu X, Gibbons J, Zhang S, Williamson P R. Copper-mediated reversal of defective laccase in a Δvph1 avirulent mutant of Cryptococcus neoformans. Mol Microbiol, 2003, 47: 1007-1014.
doi: 10.1046/j.1365-2958.2003.03340.x
[22] Anagnostakis S L. The Ecology and Physiology of the Fungal Mycelium. Cambridge: Cambridge University Press, 1984. pp 353-366.
[23] Hu Q, Min L, Yang X Y, Jin S X, Zhang L, Li Y Y, Ma Y Z, Qi X W, Li D Q, Liu H B, Lindsey K, Zhu L F, Zhang X L. Laccase GhLac1 modulates broad-spectrum biotic stress tolerance via manipulating phenylpropanoid pathway and jasmonic acid synthesis. Plant Physiol, 2018, 176: 1808-1823.
doi: 10.1104/pp.17.01628
[24] Wei T P, Tang Y, Jia P, Zeng Y, Wang B, Wu P, Quan Y G, Chen A M, Li Y C, Wu J H. A cotton lignin biosynthesis gene, GhLAC4, fine-tuned by ghr-miR397 modulates plant resistance against Verticillium dahlia. Front Plant Sci, 2021, 18: 12.
[25] Pourcel L, Routaboul J M, Kerhoas L, Caboche M, Lepiniec L, Debeaujon I. TRANSPARENT TESTA10 encodes a laccase-like enzyme involved in oxidative polymerization of flavonoids in Arabidopsis seed coat. Plant Cell, 2005, 17: 2966-2980.
doi: 10.1105/tpc.105.035154
[26] Turlapati P V, Kim K W, Davin L B, Lewis N G. The laccase multigene family in Arabidopsis thaliana: towards addressing the mystery of their gene function(s). Planta, 2011, 233: 439-470.
doi: 10.1007/s00425-010-1298-3
[27] Niladevi K N, Sukumaran R K, Prema D. Utilization of rice straw for laccase production by Streptomyces psammoticus in solid-state fermentation. J Ind Microbiol Biotechnol, 2007, 34: 665-674.
doi: 10.1007/s10295-007-0239-z
[28] Zhang R, Zhou L L, Li Y L, Ma H H, Li Y W, Ma Y Z, Lyu R J, Yang J, Wang W R, Alifu A, Zhang X L, Kong J, Min L. Rapid identification of pollen- and anther-specific genes in response to high-temperature stress based on transcriptome profiling analysis in cotton. Int J Mol Sci, 2022, 23: 3378.
doi: 10.3390/ijms23063378
[29] Min L, Zhu L F, Tu L L, Deng F L, Yuan D J, Zhang X L. Cotton GhCKI disrupts normal male reproduction by delaying tapetum programmed cell death via inactivating starch synthase. Plant J, 2013, 75: 823-835.
doi: 10.1111/tpj.2013.75.issue-5
[30] Livak K J, Schmittgen T D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods, 2001, 25: 402-408.
doi: 10.1006/meth.2001.1262 pmid: 11846609
[31] McCaig B C, Meagher R B, Dean J F D. Gene structure and molecular analysis of the laccase-like multicopper oxidase (LMCO) gene family in Arabidopsis thaliana. Planta, 2005, 221: 619-636.
doi: 10.1007/s00425-004-1472-6
[32] Dharmawardhana D P, Ellis B E, Carlson J E. Characterization of vascular lignification in Arabidopsis thaliana. Can J Bot, 1992, 70: 2238-2244.
doi: 10.1139/b92-277
[33] Naoumkina M A, Zhao Q, Gallego-Giraldo L, Dai X, Zhao P X, Dixon R A. Genome-wide analysis of phenylpropanoid defence pathways. Mol Plant Pathol, 2010, 11: 829-846.
doi: 10.1111/j.1364-3703.2010.00648.x pmid: 21029326
[34] Mottiar Y, Vanholme R, Boerjan W, Ralph J, Mansfield S D. Designer lignins: harnessing the plasticity of lignification. Curr Opin Biotechnol, 2016, 37: 190-200.
doi: 10.1016/j.copbio.2015.10.009
[35] Min L, Li Y Y, Hu Q, Zhu L F, Gao W H, Wu Y L, Ding Y H, Liu S M, Yang X Y, Zhang X L. Sugar and auxin signaling pathways respond to high-temperature stress during anther development as revealed by transcript profiling analysis in cotton. Plant Physiol, 2014, 164: 1293-1308.
doi: 10.1104/pp.113.232314 pmid: 24481135
[36] Ma Y Z, Min L, Wang M J, Wang C Z, Zhao Y L, Li Y Y, Fang Q D, Wu Y L, Xie S, Ding Y H, Su X J, Hu Q, Zhang Q H, Li X Y, Zhang X L. Disrupted genome methylation in response to high temperature has distinct affects on microspore abortion and anther indehiscence. Plant Cell, 2018, 30: 1387-1403.
doi: 10.1105/tpc.18.00074
[37] Zhao Q, Nakashima J, Chen F, Yin Y, Fu C, Yun J, Shao H, Wang X, Wang Z Y, Dixon R A. Laccase is necessary and nonredundant with peroxidase for lignin polymerization during vascular development in Arabidopsis. Plant Cell, 2013, 25: 3976-3987.
doi: 10.1105/tpc.113.117770
[38] Balasubramanian V K, Rai K M, Thu S W, Hii M M, Mendu V. Genome-wide identification of multifunctional laccase gene family in cotton (Gossypium spp.);expression and biochemical analysis during fiber development. Sci Rep, 2016, 6: 34309.
doi: 10.1038/srep34309 pmid: 27679939
[39] Johansson M, Denekamp M, Asiegbu F O. Production and isozyme pattern of extracellular laccase in the S and P intersterility groups of the root pathogen Heterobasidion annosum. Mycol Res, 1999, 103: 365-371.
doi: 10.1017/S0953756298007436
[40] Zhang Y, Wu L Z, Wang X F, Chen B, Zhao J, Cui J, Li Z K, Yang J, Wu G Y, Zhang G Y, Ma Z Y. The cotton laccase gene GhLAC15 enhances Verticillium wilt resistance via an increase in defence-induced lignification and lignin components in the cell walls of plants. Mol Plant Pathol, 2019, 20:309-322.
doi: 10.1111/mpp.12755 pmid: 30267563
[41] Torres J, Svistunenko D, Karlsson B, Cooper C E, Wilson M T. Fast reduction of a copper center in laccase by nitric oxide and formation of a peroxide intermediate. J Am Chem Soc, 2002, 124: 963-967.
pmid: 11829603
[42] 靳蓉, 张飞龙. 漆酶的结构与催化反应机理. 中国生漆, 2012, 31(4): 6-16.
Jin R, Zhang F L. Structure and catalytic mechanism of laccase. Chin Lacquer, 2012, 31(4): 6-16. (in Chinese with English abstract)
[43] Zhao Q, Nakashima J, Chen F, Yin Y, Fu C, Yun J, Shao H, Wang Z Y, Dixon R A. Laccase is necessary and nonredundant with peroxidase for lignin polymerization during vascular development in Arabidopsis. Plant Cell, 2013, 25: 3976-3987.
doi: 10.1105/tpc.113.117770
[44] Lan W, Lu F, Regner M, Zhu Y, Rencoret J, Ralph S A, Zakai U I, Morreel K, Boerjan W, Ralph J. Tricin, a flavonoid monomer in monocot lignification. Plant Physiol, 2015, 167: 1284-1295.
doi: 10.1104/pp.114.253757 pmid: 25667313
[1] MA Chun-Min, LI Wei-Xi, LI Fang-Jun, TIAN Xiao-Li, LI Zhao-Hu. Identification and expression analysis of nitrate transporter NRT gene family in upland cotton (Gossypium hirsutum L.) [J]. Acta Agronomica Sinica, 2023, 49(6): 1496-1517.
[2] XU Nai-Yin, WANG Yang, WANG Dan-Tao, NING He-Jia, YANG Xiao-Ni, QIAO Yin-Tao. Construction of cotton fiber quality index and weighted genotype by trait (WGT) biplot analysis [J]. Acta Agronomica Sinica, 2023, 49(5): 1262-1271.
[3] ZHAO Wen-Qing, XU Wen-Zheng, YANG Liu-Yan, LIU Yu, ZHOU Zhi-Guo, WANG You-Hua. Different response of cotton leaves to heat stress is closely related to the night starch degradation [J]. Acta Agronomica Sinica, 2021, 47(9): 1680-1689.
[4] XU Nai-Yin, ZHAO Su-Qin, ZHANG Fang, FU Xiao-Qiong, YANG Xiao-Ni, QIAO Yin-Tao, SUN Shi-Xian. Retrospective evaluation of cotton varieties nationally registered for the Northwest Inland cotton growing regions based on GYT biplot analysis [J]. Acta Agronomica Sinica, 2021, 47(4): 660-671.
[5] Zuo-Min WANG,Jin LIU,Shi-Chao SUN,Xin-Yu ZHANG,Fei XUE,Yan-Jun LI,Jie SUN. Identification and Expression Analysis of Multidrug and Toxic Compound Extrusion Protein Family Genes in Colored Cotton [J]. Acta Agronomica Sinica, 2018, 44(9): 1380-1392.
[6] Li-Xia QIN, Jing LI, Huan-Yang ZHANG, Sheng LI, Meng-Jie ZHU, Gai-Li JIAO, Shen-Jie WU. Cloning and Expression Analysis of Galactosyltransferase Gene GhGalT1 Promoter in Cotton [J]. Acta Agronomica Sinica, 2018, 44(02): 218-226.
Viewed
Full text


Abstract

Cited
  Shared   
  Discussed   
[1] YANG Jian-Chang;ZHANG Jian-Hua;WANG Zhi-Qin;ZH0U Qing-Sen. Changes in Contents of Polyamines in the Flag Leaf and Their Relationship with Drought-resistance of Rice Cultivars under Water Deficiency Stress[J]. Acta Agron Sin, 2004, 30(11): 1069 -1075 .
[2] TIAN Meng-Liang;HUNAG Yu-Bi;TAN Gong-Xie;LIU Yong-Jian;RONG Ting-Zhao. Sequence Polymorphism of waxy Genes in Landraces of Waxy Maize from Southwest China[J]. Acta Agron Sin, 2008, 34(05): 729 -736 .
[3] HU Xi-Yuan;LI Jian-Ping;SONG Xi-Fang. Efficiency of Spatial Statistical Analysis in Superior Genotype Selection of Plant Breeding[J]. Acta Agron Sin, 2008, 34(03): 412 -417 .
[4] Wang Yiqun. Infection of Rhizobia to Rice[J]. Acta Agronomica Sinica, 2002, 28(01): 32 -35 .
[5] KE Li-Ping;ZHENG Tao;WU Xue-Long;HE Hai-Yan;CHEN Jin-Qing. Analysis of Self-Incompatibility Locus Gene in Brassica napus[J]. Acta Agron Sin, 2008, 34(05): 764 -769 .
[6] CUI Xiu-Hui. Male Sterility Induced by Chemical Hybridizing Agent SQ-1 in Common Millet[J]. Acta Agron Sin, 2008, 34(01): 106 -110 .
[7] A JIA La-Tie;ZENG Long-Jun;XUE Da-Wei;HU Jiang;ZENG Da-Li;GAO Zhen-Yu;GUO Long-Biao;LI Shi-Gui;QIAN Qian
. QTL Analysis for Chlorophyll Content in Four Grain-Filling Stage in Rice[J]. Acta Agron Sin, 2008, 34(01): 61 -66 .
[8] YANG Wen-Xiong;YANG Fang-Ping;LIANG Dan;HE Zhong-Hu;SHANG Xun-Wu;XIA Xian-Chun. Molecular Characterization of Slow-Rusting Genes Lr34/Yr18 in Chinese Wheat Cultivars[J]. Acta Agron Sin, 2008, 34(07): 1109 -1113 .
[9] WANG Ying;WU Cun-Xiang;ZHANG Xue-Ming;WANG Yun-Peng;HAN Tian-Fu. Effects of Soybean Major Maturity Genes under Different Photoperiods[J]. Acta Agron Sin, 2008, 34(07): 1160 -1168 .
[10] WANG Guo-Li;GUO Zhen-Fei. Effects of Phosphorus Nutrient on the Photosynthetic Characteristics in Rice Cultivars with Different Cold-Sensitivity[J]. Acta Agron Sin, 2007, 33(08): 1385 -1389 .
Add: No. 80 Xueyuan South Rd, Beijing 100081, P. R. China E-mail: zwxb301@caas.cn
Supported by Beijing Magtech Co.Ltd