Characterization and validation of TaAGL66, a gene related to fertility conversion of wheat in the presence of Aegilops kotschyi cytoplasm.
Aegilops kotschyi
TaAGL66
Hybrid wheat
MADS-box transcription factor
Thermo-sensitive cytoplasmic male sterility
Journal
Planta
ISSN: 1432-2048
Titre abrégé: Planta
Pays: Germany
ID NLM: 1250576
Informations de publication
Date de publication:
23 May 2024
23 May 2024
Historique:
received:
16
01
2024
accepted:
15
04
2024
medline:
23
5
2024
pubmed:
23
5
2024
entrez:
23
5
2024
Statut:
epublish
Résumé
TaAGL66, a MADS-box transcription factor highly expressed in fertile anthers of KTM3315A, regulates anther and/or pollen development, as well as male fertility in wheat with Aegilops kotschyi cytoplasm. Male sterility, as a string of sophisticated biological processes in higher plants, is commonly regulated by transcription factors (TFs). Among them, MADS-box TFs are mainly participated in the processes of floral organ formation and pollen development, which are tightly related to male sterility, but they have been little studied in the reproductive development in wheat. In our study, TaAGL66, a gene that was specifically expressed in spikes and highly expressed in fertile anthers, was identified by RNA sequencing and the expression profiles data of these genes, and qRT-PCR analyses, which was localized to the nucleus. Silencing of TaAGL66 under fertility condition in KTM3315A, a thermo-sensitive male sterile line with Ae. kotschyi cytoplasm, displayed severe fertility reduction, abnormal anther dehiscence, defective pollen development, decreased viability, and low seed-setting. It can be concluded that TaAGL66 plays an important role in wheat pollen development in the presence of Ae. kotschyi cytoplasm, providing new insights into the utilization of male sterility.
Identifiants
pubmed: 38780795
doi: 10.1007/s00425-024-04416-z
pii: 10.1007/s00425-024-04416-z
doi:
Substances chimiques
Plant Proteins
0
MADS Domain Proteins
0
Transcription Factors
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
6Subventions
Organisme : National Natural Science Foundation of China
ID : 32072060
Organisme : National Natural Science Foundation of China
ID : 32372183
Organisme : Key R&D Program of Yangling Seed Industry Innovation Center
ID : Ylzy-xm-03
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Adamczyk BJ, Fernandez DE (2009) MIKC* MADS domain heterodimers are required for pollen maturation and tube growth in Arabidopsis. Plant Physiol 149(4):1713–1723
pubmed: 19211705
pmcid: 2663741
doi: 10.1104/pp.109.135806
Chen L, Yang W, Liu S, Meng Y, Zhu Z, Liang R, Cao K, Xie Y, Li X (2023) Genome-wide analysis and identification of light-harvesting chlorophyll a/b binding (LHC) gene family and BSMV-VIGS silencing TaLHC86 reduced salt tolerance in wheat. Int J Biol Macromol 242(3):124930
pubmed: 37236564
doi: 10.1016/j.ijbiomac.2023.124930
Colombo L, Franken J, Koetje E, van Went J, Dons HJ, Angenent GC, van Tunen AJ (1995) The petunia MADS box gene FBP11 determines ovule identity. Plant Cell 7(11):1859–1868
pubmed: 8535139
pmcid: 161044
Dan Z, Chen Y, Zhao W, Wang Q, Huang W (2019) Metabolome-based prediction of yield heterosis contributes to the breeding of elite rice. Life Sci Alliance 3(1):e201900551
pubmed: 31836628
pmcid: 6918511
doi: 10.26508/lsa.201900551
Davies B, Schwarz-Sommer Z (1994) Control of floral organ identity by homeotic MADS-box transcription factors. Results Probl Cell Differ 20:235–258
pubmed: 7913550
doi: 10.1007/978-3-540-48037-2_11
De Bodt S, Raes J, Florquin K, Rombauts S, Rouze P, Theissen G, Van de Peer Y (2003) Genomewide structural annotation and evolutionary analysis of the type I MADS-box genes in plants. J Mol Evol 56:573–586
pubmed: 12698294
doi: 10.1007/s00239-002-2426-x
Dommes AB, Gross T, Herbert DB, Kivivirta KI, Becker A (2019) Virus-induced gene silencing: empowering genetics in non-model organisms. J Exp Bot 70(3):757–770
pubmed: 30452695
doi: 10.1093/jxb/ery411
Fernández-Gómez J, Talle B, Wilson ZA (2020) Increased expression of the MALE STERILITY1 transcription factor gene results in temperature-sensitive male sterility in barley. J Exp Bot 71(20):6328–6339
pubmed: 32860504
pmcid: 7586743
doi: 10.1093/jxb/eraa382
Gao H, Wang Z, Li S, Hou M, Zhou Y, Zhao Y, Li G, Zhao H, Ma H (2018) Genome-wide survey of potato MADS-box genes reveals that StMADS1 and StMADS13 are putative downstream targets of tuberigen StSP6A. BMC Genomics 19(1):726
pubmed: 30285611
pmcid: 6171223
doi: 10.1186/s12864-018-5113-z
Geng X, Wang X, Wang J, Yang X, Zhang L, Song X (2021) TaEXPB5 functions as a gene related to pollen development in thermo-sensitive male-sterility wheat with Aegilops kotschyi cytoplasm. Plant Sci 323:111377
doi: 10.1016/j.plantsci.2022.111377
Gimenez E, Castañeda L, Pineda B, Pan IL, Moreno V, Angosto T, Lozano R (2016) TOMATO AGAMOUS1 and ARLEQUIN/TOMATO AGAMOUS-LIKE1 MADS-box genes have redundant and divergent functions required for tomato reproductive development. Plant Mol Biol 91(4–5):513–531
pubmed: 27125648
doi: 10.1007/s11103-016-0485-4
Gimenez K, Blanc P, Argillier O, Pierre JB, Le Gouis J, Paux E (2021) Dissecting bread wheat heterosis through the integration of agronomic and physiological traits. Biology (basel) 10(9):907
pubmed: 34571784
pmcid: 8465846
Groszyk J, Kowalczyk M, Yanushevska Y, Stochmal A, Rakoczy-Trojanowska M, Orczyk W (2017) Identification and VIGS-based characterization of Bx1 ortholog in rye (Secale cereale L.). PLoS One 12(2):e0171506
pubmed: 28234909
pmcid: 5325281
doi: 10.1371/journal.pone.0171506
Gunupuru LR, Perochon A, Ali SS, Scofield SR, Doohan FM (2019) Virus-induced gene silencing (VIGS) for functional characterization of disease resistance genes in barley seedlings. Methods Mol Biol 1900:95–114
pubmed: 30460561
doi: 10.1007/978-1-4939-8944-7_7
Guo Y, Gan S (2006) AtNAP, a NAC family transcription factor, has an important role in leaf Senescence. Plant J 46(4):601–612
pubmed: 16640597
doi: 10.1111/j.1365-313X.2006.02723.x
Han Y, Zhao F, Gao S, Wang X, Wei A, Chen Z, Liu N, Tong X, Fu X, Wen C, Zhang Z, Wang N, Du S (2018) Fine mapping of a male sterility gene ms-3 in a novel cucumber (Cucumis sativus L.) mutant. Theor Appl Genet 131(2):449–460
pubmed: 29134240
doi: 10.1007/s00122-017-3013-2
Han Y, Gao Y, Zhou H, Zhai X, Ding Q, Ma L (2021) Mitochondrial genes are involved in the fertility transformation of the thermosensitive male-sterile line YS3038 in wheat. Mol Breed 41(10):61
pubmed: 37309316
pmcid: 10236089
doi: 10.1007/s11032-021-01252-x
Han Y, Gao Y, Li Y, Zhai X, Zhou H, Ding Q, Ma L (2022) Chloroplast genes are involved in the male-sterility of K-type CMS in wheat. Genes (basel) 13(2):310
pubmed: 35205355
pmcid: 8871828
doi: 10.3390/genes13020310
Kaufmann K, Melzer R, Theißen G (2005) MIKC-type MADS-domain proteins: Structural modularity, protein interactions and network evolution in land plants. Gene 347:183–198
pubmed: 15777618
doi: 10.1016/j.gene.2004.12.014
Kong X, Wang F, Geng S, Guan J, Tao S, Jia M, Sun G, Wang Z, Wang K, Ye X (2022) The wheat AGL6-like MADS-box gene is a master regulator for floral organ identity and a target for spikelet meristem development manipulation. Plant Biotechnol J 20:75–88
pubmed: 34487615
doi: 10.1111/pbi.13696
Li H, Liang W, Hu Y, Zhu L, Yin C, Xu J, Dreni L, Kater MM, Zhang D (2011) Rice MADS6 interacts with the floral homeotic genes SUPERWOMAN1, MADS3, MADS58, MADS13, and DROOPING LEAF in specifying floral organ identities and meristem fate. Plant Cell 23(7):2536–2552
pubmed: 21784949
pmcid: 3226212
doi: 10.1105/tpc.111.087262
Li G, Kuijer HNJ, Yang X, Liu H, Shen C, Shi J, Betts N, Tucker MR, Liang W, Waugh R, Burton RA, Zhang D (2021) MADS1 maintains barley spike morphology at high ambient temperatures. Nat Plants 7(8):1093–1107
pubmed: 34183784
doi: 10.1038/s41477-021-00957-3
Liang Q, Shang L, Wang Y, Hua J (2015) Partial dominance, overdominance and epistasis as the genetic basis of heterosis in upland cotton (Gossypium hirsutum L.). PLoS One 10(11):e0143548
pubmed: 26618635
pmcid: 4664285
doi: 10.1371/journal.pone.0143548
Liu Y, Cui S, Wu F, Yan S, Lin X, Du X, Chong K, Schilling S, Theißen G, Meng Z (2013) Functional conservation of MIKC*-type MADS box genes in Arabidopsis and rice pollen maturation. Plant Cell 25(4):1288–1303
pubmed: 23613199
pmcid: 3663268
doi: 10.1105/tpc.113.110049
Luo JH, Wang M, Jia GF, He Y (2021) Transcriptome-wide analysis of epitranscriptome and translational efficiency associated with heterosis in maize. J Exp Botany 72(8):2933–2946
doi: 10.1093/jxb/erab074
Ma J, Yang Y, Luo W, Yang C, Ding P, Liu Y, Qiao L, Chang Z, Geng H, Wang P, Jiang Q, Wang J, Chen G, Wei Y, Zheng Y, Lan X (2017) Genome-wide identification and analysis of the MADS-box gene family in bread wheat (Triticum aestivum L.). PLoS ONE 12(7):e0181443
pubmed: 28742823
pmcid: 5526560
doi: 10.1371/journal.pone.0181443
Meng L, Liu Z, Zhang L, Hu G, Song X (2016) Cytological characterization of a thermo-sensitive cytoplasmic male-sterile wheat line having K-type cytoplasm of Aegilops kotschyi. Breed Sci 66(5):752–761
pubmed: 28163591
pmcid: 5282749
doi: 10.1270/jsbbs.16039
Münster T, Wingen LU, Faigl W, Werth S, Saedler H, Theissen G (2001) Characterization of three GLOBOSA-like MADS-box genes from maize: evidence for ancient paralogy in one class of floral homeotic B-function genes of grasses. Gene 262(1–2):1–13
pubmed: 11179662
doi: 10.1016/S0378-1119(00)00556-4
Nascimento FF, Reis MD, Yang Z (2017) A biologist’s guide to Bayesian phylogenetic analysis. Nat Ecol Evol 1(10):1446–1454
pubmed: 28983516
pmcid: 5624502
doi: 10.1038/s41559-017-0280-x
Pacak A, Geisler K, Jørgensen B, Barciszewska-Pacak M, Nilsson L, Nielsen TH, Johansen E, Grønlund M, Jakobsen I, Albrechtsen M (2010) Investigations of barley stripe mosaic virus as a gene silencing vector in barley roots and in Brachypodium distachyon and oat. Plant Methods 6:26
pubmed: 21118486
pmcid: 3006357
doi: 10.1186/1746-4811-6-26
Parenicová L, de Folter S, Kieffer M, Horner DS, Favalli C, Busscher J, Cook HE, Ingram RM, Kater MM, Davies B, Angenent GC, Colombo L (2003) Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell 15(7):1538–1551
pubmed: 12837945
pmcid: 165399
doi: 10.1105/tpc.011544
Ranjan R, Malik N, Sharma S, Agarwal P, Kapoor S, Tyagi AK (2022) OsCPK29 interacts with MADS68 to regulate pollen development in rice. Plant Sci 321:111297
pubmed: 35696904
doi: 10.1016/j.plantsci.2022.111297
Saha G, Park JI, Jung HJ, Ahmed NU, Kayum MA, Chung MY, Hur Y, Cho YG, Watanabe M, Nou IS (2015) Genome-wide identification and characterization of MADS-box family genes related to organ development and stress resistance in Brassica rapa. BMC Genomics 16(1):178
pubmed: 25881193
pmcid: 4422603
doi: 10.1186/s12864-015-1349-z
Shi X, Li W, Guo Z, Wu M, Zhang X, Yuan L, Qiu X, Xing Y, Sun X, Xie H, Tang J (2022) Comparative transcriptomic analysis of maize ear heterosis during the inflorescence meristem differentiation stage. BMC Plant Biol 22(1):348
pubmed: 35843937
pmcid: 9290290
doi: 10.1186/s12870-022-03695-6
Wu J, Peng Z, Liu S, He Y, Cheng L, Kong F, Wang J, Lu G (2012) Genome-wide analysis of Aux/IAA gene family in Solanaceae species using tomato as a model. Mol Genet Genomics 287(4):295–311
pubmed: 22314799
doi: 10.1007/s00438-012-0675-y
Wu B, Xia Y, Zhang G, Wang J, Ma S, Song Y, Yang Z, Dennis ES, Niu N (2022) The transcription factors TaTDRL and TaMYB103 synergistically activate the expression of TAA1a in wheat, which positively regulates the development of microspore in Arabidopsis. Int J Mol Sci 23(14):7996
pubmed: 35887343
pmcid: 9321142
doi: 10.3390/ijms23147996
Xiang XJ, Sun LP, Yu P, Yang ZF, Zhang PP, Zhang YX, Wu WX, Chen DB, Zhan XD, Khan RM, Abbas A, Cheng SH, Cao LY (2021) The MYB transcription factor Baymax1 plays a critical role in rice male fertility. Theor Appl Genet 134(2):453–471
pubmed: 33089345
doi: 10.1007/s00122-020-03706-w
Xu Y, Yu D, Chen J, Duan M (2023) A review of rice male sterility types and their sterility mechanisms. Heliyon 9(7):e18204
pubmed: 37519640
pmcid: 10372310
doi: 10.1016/j.heliyon.2023.e18204
Yang W, Lou X, Li J, Pu M, Mirbahar AA, Liu D, Sun J, Zhan K, He L, Zhang A (2017) Cloning and functional analysis of MADS-box genes, TaAG-A and TaAG-B, from a wheat K-type cytoplasmic male sterile line. Front Plant Sci 8:1081
pubmed: 28676817
pmcid: 5476771
doi: 10.3389/fpls.2017.01081
Yang X, Geng X, Liu Z, Ye J, Zhang L, Song X (2018) A sterility induction trait in the genic male sterility wheat line 4110S induced by high temperature and its cytological response. Crop Sci 58:1–11
doi: 10.2135/cropsci2017.12.0714
Yoo SK, Lee JS, Ahn JH (2006) Overexpression of AGAMOUS-LIKE 28 (AGL28) promotes flowering by upregulating expression of floral promoters within the autonomous pathway. Biochem Biophys Res Commun 348(3):929–936
pubmed: 16899218
doi: 10.1016/j.bbrc.2006.07.121
Zhang ZB, Zhu J, Gao JF, Wang C, Li H, Li H, Zhang HQ, Zhang S, Wang DM, Wang QX, Huang H, Xia HJ, Yang ZN (2007) Transcription factor AtMYB103 is required for anther development by regulating tapetum development, callose dissolution and exine formation in Arabidopsis. Plant J 52(3):528–538
pubmed: 17727613
doi: 10.1111/j.1365-313X.2007.03254.x
Zhao ML, Zhou ZF, Chen MS, Xu CJ, Xu ZF (2022) An ortholog of the MADS-box gene SEPALLATA3 regulates stamen development in the woody plant Jatropha curcas. Planta 255(6):111
pubmed: 35478059
doi: 10.1007/s00425-022-03886-3