Conservation and diversification of HAIRY MERISTEM gene family in land plants.


Journal

The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397

Informations de publication

Date de publication:
04 2021
Historique:
revised: 07 01 2021
received: 29 10 2020
accepted: 18 01 2021
pubmed: 24 1 2021
medline: 25 8 2021
entrez: 23 1 2021
Statut: ppublish

Résumé

The shoot apical meristems (SAMs) of land plants are crucial for plant growth and organ formation. In several angiosperms, the HAIRY MERISTEM (HAM) genes function as key regulators that control meristem development and stem cell homeostasis. To date, the origin and evolutionary history of the HAM family in land plants remains unclear. Potentially shared and divergent functions of HAM family members from angiosperms and non-angiosperms are also not known. In constructing a comprehensive phylogeny of the HAM family, we show that HAM proteins are widely present in land plants and that HAM proteins originated prior to the divergence of bryophytes. The HAM family was duplicated in a common ancestor of angiosperms, leading to two distinct groups: type I and type II. Type-II HAM members are widely present in angiosperms, whereas type-I HAM members were independently lost in different orders of monocots. Furthermore, HAM members from angiosperms and non-angiosperms (including bryophytes, lycophytes, ferns and gymnosperms) are able to replace the role of the type-II HAM genes in Arabidopsis, maintaining established SAMs and promoting the initiation of new stem cell niches. Our results uncover the conserved functions of HAM family members and reveal the conserved regulatory mechanisms underlying HAM expression patterning in meristems, providing insight into the evolution of key stem cell regulators in land plants.

Identifiants

pubmed: 33484592
doi: 10.1111/tpj.15169
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

366-378

Informations de copyright

© 2021 Society for Experimental Biology and John Wiley & Sons Ltd.

Références

Amborella Genome Project (2013) The Amborella genome and the evolution of flowering plants. Science, 342, 1241089.
Aya, K., Kobayashi, M., Tanaka, J., Ohyanagi, H., Suzuki, T., Yano, K. et al. (2014) De Novo transcriptome assembly of a fern, Lygodium japonicum, and a web resource database, Ljtrans DB. Plant and Cell Physiology, 56, e5.
Banks, J.A., Nishiyama, T., Hasebe, M., Bowman, J.l, Gribskov, M., dePamphilis, C. et al. (2011) The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science, 332, 960.
Barrell, P.J. & Conner, A.J. (2006) Minimal T-DNA vectors suitable for agricultural deployment of transgenic plants. BioTechniques, 41, 708-710.
Bierhorst, D.W. (1977) On the stem apex, leaf initiation and early leaf ontogeny in filicalean ferns. American Journal of Botany, 64, 125-152.
Bolle, C. (2016) Chapter 19 - Functional aspects of GRAS family proteins. Plant Transcription Factors (Gonzalez, D.H edition. (Boston, Academic Press), pp. 295-311.
Bowman, J.L., Kohchi, T., Yamato, K.T. et al. (2017) Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell, 171, 287-304.e215.
Cai, C., Lanman, N.A., Withers, K.A., DeLeon, A.M., Wu, Q., Gribskov, M. et al. (2019) Three genes define a bacterial-like arsenic tolerance mechanism in the arsenic hyperaccumulating fern Pteris vittata. Current Biology, 29, 1625-1633.e1623.
Cheng, S., Xian, W., Fu, Y., Marin, B., Keller, J., Wu, T. et al. (2019) Genomes of subaerial Zygnematophyceae provide insights into land plant evolution. Cell, 179, 1057-1067.e1014.
Clough, S.J. & Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium -mediated transformation of Arabidopsis thaliana. The Plant Journal, 16, 735-743.
Crooks, G.E., Hon, G., Chandonia, J.M. & Brenner, S.E. (2004) WebLogo: a sequence logo generator. Genome Research, 14, 1188-1190.
David-Schwartz, R., Borovsky, Y., Zemach, H. & Paran, I. (2013) CaHAM is autoregulated and regulates CaSTM expression and is required for shoot apical meristem organization in pepper. Plant Science, 203-204, 8-16.
Engstrom, E.M., Andersen, C.M., Gumulak-Smith, J., Hu, J., Orlova, E., Sozzani, R. et al. (2011) Arabidopsis homologs of the Petunia HAIRY MERISTEM gene are required for maintenance of shoot and root indeterminacy. Plant Physiology, 155, 735-750.
Fan, T., Li, X., Yang, W., Xia, K., Ouyang, J. & Zhang, M. (2015) Rice osa-miR171c mediates phase change from vegetative to reproductive development and shoot apical meristem maintenance by repressing four OsHAM transcription factors. PLoS One, 10, e0125833.
Frangedakis, E., Saint-Marcoux, D., Moody, L.A., Rabbinowitsch, E. & Langdale, J.A. (2017) Nonreciprocal complementation of KNOX gene function in land plants. New Phytologist, 216, 591-604.
Fu, L., Niu, B., Zhu, Z., Wu, S. & Li, W. (2012) CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics (Oxford, England), 28, 3150-3152.
Gaillochet, C. & Lohmann, J.U. (2015) The never-ending story: from pluripotency to plant developmental plasticity. Development, 142, 2237.
Geng, Y. & Zhou, Y. (2019) Confocal live imaging of shoot apical meristems from different plant species. JoVE, e59369.
Guo, P., Wen, J., Yang, J., Ke, Y., Wang, M., Liu, M. et al. (2019) Genome-wide survey and expression analyses of the GRAS gene family in Brassica napus reveals their roles in root development and stress response. Planta, 250, 1051-1072.
Han, H., Geng, Y., Guo, L., Yan, A., Meyerowitz, E.M., Liu, X., et al. (2020a) The overlapping and distinct roles of HAM family genes in Arabidopsis shoot meristems. Front Plant Science, 11.
Han, H., Liu, X. & Zhou, Y. (2020b) Transcriptional circuits in control of shoot stem cell homeostasis. Current Opinion in Plant Biology, 53, 50-56.
Han, H., Yan, A., Li, L., Zhu, Y., Feng, B., Liu, X. & et al. (2020c) A signal cascade originated from epidermis defines apical-basal patterning of Arabidopsis shoot apical meristems. Nature Communications, 11, 1214.
Hendelman, A., Kravchik, M., Stav, R., Frank, W. & Arazi, T. (2016) Tomato HAIRY MERISTEM genes are involved in meristem maintenance and compound leaf morphogenesis. Journal of Experimental Botany, 67, 6187-6200.
Imaichi, R. & Hiratsuka, R. (2007) Evolution of shoot apical meristem structures in vascular plants with respect to plasmodesmatal network. American Journal of Botany, 94, 1911-1921.
Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 587.
Katoh, K., Kuma, K.-I., Toh, H. & Miyata, T. (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research, 33, 511-518.
Lang, D., Ullrich, K.K., Murat, F. et al. (2018) The Physcomitrella patens chromosome-scale assembly reveals moss genome structure and evolution. The Plant Journal, 93, 515-533.
Leebens-Mack, J.H., Barker, M.S., Carpenter, E.J. et al. (2019) One thousand plant transcriptomes and the phylogenomics of green plants. Nature, 574, 679-685.
Letunic, I. & Bork, P. (2019) Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Research, 47, W256-W259.
Li, F.-W., Brouwer, P., Carretero-Paulet, L. et al. (2018) Fern genomes elucidate land plant evolution and cyanobacterial symbioses. Nat Plants., 4, 460-472.
Li, W.-F., Zhang, S.-G., Han, S.-Y., Wu, T., Zhang, J.-H. & Qi, L.-W. (2014) The post-transcriptional regulation of LaSCL6 by miR171 during maintenance of embryogenic potential in Larix kaempferi (Lamb.) Carr. Tree Genetics and Genomes, 10, 223-229.
Li, W., Zhou, Y., Liu, X., Yu, P., Cohen, J.D. & Meyerowitz, E.M. (2013) LEAFY controls auxin response pathways in floral primordium formation. Science Signalling, 6, ra23-ra23.
Llave, C., Xie, Z., Kasschau, K.D. & Carrington, J.C. (2002) Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science, 297, 2053.
Maizel, A., Busch, M.A., Tanahashi, T., Perkovic, J., Kato, M., Hasebe, M., et al. (2005) The floral regulator LEAFY evolves by substitutions in the DNA binding domain. Science, 308, 260.
Meyerowitz, E.M. (1997) Genetic control of cell division patterns in developing plants. Cell, 88, 299-308.
Minh, B.Q., Nguyen, M.A.T. & von Haeseler, A. (2013) Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution, 30, 1188-1195.
Neale, D.B., McGuire, P.E., Wheeler, N.C. et al. (2017) The douglas-fir genome sequence reveals specialization of the photosynthetic apparatus in Pinaceae. G3-Genes Genom. Genet., 7, 3157.
Neale, D.B., Wegrzyn, J.L., Stevens, K.A., Zimin, A.V., Puiu, D., Crepeau, M.W. et al. (2014) Decoding the massive genome of loblolly pine using haploid DNA and novel assembly strategies. Genome Biology, 15, R59.
Nguyen, L.-T., Schmidt, H.A., von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies. Molecular Biology and Evolution, 32, 268-274.
Plackett, A.R.G., Di Stilio, V.S. & Langdale, J.A. (2015) Ferns: the missing link in shoot evolution and development. Front Plant Science, 6.
Prunet, N. (2017) Live confocal imaging of developing Arabidopsis flowers. JoVE, e55156.
Rhoades, M.W., Reinhart, B.J., Lim, L.P., Burge, C.B., Bartel, B. & Bartel, D.P. (2002) Prediction of plant microRNA targets. Cell, 110, 513-520.
Sablowski, R. (2007) The dynamic plant stem cell niches. Current Opinion in Plant Biology, 10, 639-644.
Schoof, H., Lenhard, M., Haecker, A., Mayer, K.F.X., Jürgens, G. & Laux, T. (2000) The stem cell population of arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell, 100, 635-644.
Schulze, S., Schäfer, B.N., Parizotto, E.A., Voinnet, O. & Theres, K. (2010) LOST MERISTEMS genes regulate cell differentiation of central zone descendants in Arabidopsis shoot meristems. The Plant Journal, 64, 668-678.
Stuurman, J., Jäggi, F. & Kuhlemeier, C. (2002) Shoot meristem maintenance is controlled by a GRAS-gene mediated signal from differentiating cells. Genes & Development, 16, 2213-2218.
Tian, C., Wan, P., Sun, S., Li, J. & Chen, M. (2004) Genome-wide analysis of the GRAS gene family in rice and Arabidopsis. Plant Molecular Biology, 54, 519-532.
Wang, L., Mai, Y.-X., Zhang, Y.-C., Luo, Q. & Yang, H.-Q. (2010) MicroRNA171c-targeted SCL6-II, SCL6-III, and SCL6-IV genes regulate shoot branching in Arabidopsis. Mol Plant, 3, 794-806.
Wang, Y.-X., Liu, Z.-W., Wu, Z.-J., Li, H., Wang, W.-L., Cui, X. et al. (2018) Genome-wide identification and expression analysis of GRAS family transcription factors in tea plant (Camellia sinensis). Scientific Reports, 8, 3949.
Zhang, Y., Jiao, Y., Jiao, H., Zhao, H. & Zhu, Y.-X. (2017) Two-step functional innovation of the stem-cell factors WUS/WOX5 during plant evolution. Molecular Biology and Evolution, 34, 640-653.
Zhou, Y., Liu, X., Engstrom, E.M., Nimchuk, Z.L., Pruneda-Paz, J.L., Tarr, P.T. et al. (2015) Control of plant stem cell function by conserved interacting transcriptional regulators. Nature, 517, 377.
Zhou, Y., Yan, A., Han, H., Li, T., Geng, Y., Liu, X. et al. (2018) HAIRY MERISTEM with WUSCHEL confines CLAVATA3 expression to the outer apical meristem layers. Science, 361, 502.

Auteurs

Yuan Geng (Y)

Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN, 47907, USA.
Purdue Center for Plant Biology, Purdue University, West Lafayette, IN, 47907, USA.

Lei Guo (L)

Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN, 47907, USA.
Purdue Center for Plant Biology, Purdue University, West Lafayette, IN, 47907, USA.

Han Han (H)

Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN, 47907, USA.
Purdue Center for Plant Biology, Purdue University, West Lafayette, IN, 47907, USA.

Xing Liu (X)

Purdue Center for Plant Biology, Purdue University, West Lafayette, IN, 47907, USA.
Department of Biochemistry, Purdue University, West Lafayette, IN, 47907, USA.

Jo Ann Banks (JA)

Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN, 47907, USA.
Purdue Center for Plant Biology, Purdue University, West Lafayette, IN, 47907, USA.

Jennifer H Wisecaver (JH)

Purdue Center for Plant Biology, Purdue University, West Lafayette, IN, 47907, USA.
Department of Biochemistry, Purdue University, West Lafayette, IN, 47907, USA.

Yun Zhou (Y)

Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN, 47907, USA.
Purdue Center for Plant Biology, Purdue University, West Lafayette, IN, 47907, USA.

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