Genetic analyses of embryo homology and ontogeny in the model grass Zea mays subsp. mays.
coleoptile
embryo
grasses
homology
maize
scutellum
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
24 Jun 2024
24 Jun 2024
Historique:
received:
05
04
2024
accepted:
06
06
2024
medline:
26
6
2024
pubmed:
26
6
2024
entrez:
26
6
2024
Statut:
aheadofprint
Résumé
The homology of the single cotyledon of grasses and the ontogeny of the scutellum and coleoptile as the initial, highly modified structures of the grass embryo are investigated using leaf developmental genetics and targeted transcript analyses in the model grass Zea mays subsp. mays. Transcripts of leaf developmental genes are identified in both the initiating scutellum and the coleoptile, while mutations disrupting mediolateral leaf development also disrupt scutellum and coleoptile morphology, suggesting that these grass-specific organs are modified leaves. Higher-order mutations in WUSCHEL-LIKE HOMEOBOX3 (WOX3) genes, involved in mediolateral patterning of plant lateral organs, inform a model for the fusion of coleoptilar margins during maize embryo development. Genetic, RNA-targeting, and morphological evidence supports models for cotyledon evolution where the scutellum and coleoptile, respectively, comprise the distal and proximal domains of the highly modified, single grass cotyledon.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Division of Integrative Organismal Systems
ID : 2210259
Organisme : Directorate for Biological Sciences
ID : NSF IOS-2016021
Informations de copyright
© 2024 The Authors. New Phytologist © 2024 New Phytologist Foundation.
Références
Abbe EC, Stein OL. 1954. The growth of the shoot apex in maize: embryogeny. American Journal of Botany 41: 285–293.
Anderson MJ. 2001. A new method for non‐parametric multivariate analysis of variance: non‐parametric ANOVA for ecology. Austral Ecology 26: 32–46.
Bossinger G, Lundquist U, Salamini F. 1992. Genetics of plant development in barley. Barley Genetics 2: 989–1022.
Boyd L. 1931. Evolution in the monocotyledonous seedling: A new interpretation of the morphology of the grass embryo. Transactions of the Botanical Society of Edinburgh 30: 286–303.
Burger WC. 1998. The question of cotyledon homology in angiosperms. Botanical Review 64: 356–371.
Campbell DH. 1930. The phylogeny of monocotyledons. Annals of Botany 44: 311–331.
Chandler JW. 2008. Cotyledon organogenesis. Journal of Experimental Botany 59: 2917–2931.
Claude J. 2008. Morphometrics with R. New York, NY, USA: Springer.
Cronquist A. 1988. The evolution and classification of flowering plants, 2nd edn. New York, NY, USA: New York Botanical Garden.
Dean E. 2002. Upcoming changes in flowering plant family names: those pesky taxonomists are at it again! Fremontia 30: 3–12.
Fu YB. 2024. Polycotyly: how little do we know? Plants 13: 1054.
Haines RW, Lye KA. 1979. Monocotylar seedlings: a review of evidence supporting an origin by fusion. Botanical Journal of the Linnaean Society 78: 123–140.
Hill AW. 1906. The morphology and seedling structure of the geophilous species of peperomia, together with some views on the origin of monocotyledons. Annals of Botany 20: 395–427.
Iwata H, Ukai Y. 2002. Shape: a computer program package for quantitative evaluation of biological shapes based on elliptic Fourier descriptors. The Journal of Heredity 93: 384–385.
Jackson D. 1991. In situ hybridization in plants. In: Bowles DJ, Gurr SJ, McPherson M, eds. Molecular plant pathology: a practical approach. Oxford, UK: Oxford University Press.
Kaplan DR. 1984. Cladistics: perspectives on the reconstruction of evolutionary history. New York, NY, USA: Columbia University Press.
Kaplan DR, Cooke TJ. 1997. Fundamental concepts in the embryogenesis of dicotyledons: a morphological interpretation of embryo mutants. Plant Cell 9: 1903–1919.
Kaplan DR, Specht CD. 2022. Kaplan's principles of plant morphology. New York, NY, USA: CRC Press.
Kausch AP, Wang K, Kaeppler HF, Gordon‐Kamm W. 2021. Maize transformation: history, progress, and perspectives. Molecular Breeding 41: 38.
Kiesselbach TA. 1949. The structure and reproduction of corn. University of Nebraska Agriculture of Statistic Research Bulletin 161: 1–96.
Langdale JA, Zelitch I, Miller E, Nelson T. 1988. Cell position and light influence C4 versus C3 patterns of photosynthetic gene expression in maize. EMBO Journal 7: 3643–3651.
Leiboff S, DeAllie CK, Scanlon MJ. 2016. Modeling the morphometric evolution of the maize shoot apical meristem. Frontiers in Plant Science 7: 1651.
Nardmann J, Ji J, Werr W, Scanlon MJ. 2004. The maize duplicate genes narrow sheath1 and narrow sheath2 encode a conserved homeobox gene function in a lateral domain of shoot apical meristems. Development 131: 2827–2839.
Niklas KJ. 2008. Embryo morphology and seedling evolution. In: Leck MA, ed. Seedling ecology and evolution. Cambridge, UK: Cambridge University Press, 103–129.
Poethig RS. 1984. Cellular parameters of leaf morphogenesis in maize and tobacco. In: White R, Dickison W, eds. Contemporary problems in plant anatomy. New York, NY, USA: Academic Press, 235–238.
Ray J. 1686. Historia plantarum. London, UK: The Royal Society.
Rohatgi A. 2022. WebPlotDigitizer (v.4.6). [WWW document] URL https://automeris.io/WebPlotDigitizer.html [accessed 16 September 2022].
Sargent E. 1903. A theory of the origin of monocotyledons found on the structure of their seedlings. Annals of Botany 17: 1–92.
Satterlee JW, Evans LJ, Conlon BR, Conklin P, Martinez‐Gomez J, Yen JR, Wu H, Sylvester AW, Specht CD, Cheng J et al. 2023. A Wox3‐patterning module organizes planar growth in grass leaves and ligules. Nature Plants 9: 720–732.
Satterlee JW, Strable J, Scanlon MJ. 2020. Plant stem‐cell organization and differentiation at single‐cell resolution. Proceedings of the National Academy of Sciences, USA 117: 33689–33699.
Scanlon MJ. 2003. The polar auxin transport inhibitor N‐1‐naphthylphthalamic acid disrupts leaf initiation, KNOX protein regulation, and formation of leaf margins in maize. Plant Physiology 133: 597–605.
Scanlon MJ, Freeling M. 1998. The narrow sheath leaf domain deletion : a genetic tool used to reveal developmental homologies among modified maize organs. The Plant Journal 13: 547–561.
Scanlon MJ, Schneeberger RG, Freeling M. 1996. The maize mutant narrow sheath fails to establish leaf margin identity in a meristematic domain. Development 122: 1683–1691.
Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA et al. 2009. The B73 maize genome: complexity, diversity, and dynamics. Science 26: 1112–1115.
Strable J, Yen JR, Scanlon MJ, Sylvester AW. 2020. Toluidine Blue O staining of paraffin‐sectioned maize tissue. Bio‐Protocol 101: e3612.
Takacs EM, Li J, Du C, Ponnala L, Janick‐Buckner D, Yu J, Muehlbauer GJ, Schnable PS, Timmermans MC, Sun Q et al. 2012. Ontogeny of the maize shoot apical meristem. Plant Cell 24: 3219–3234.
Tillich HJ. 1990. The seedlings of Nymphaeaceae: monocotylar or dicotylar? Flora 184: 169–176.
Titova GE, Batygina TB. 1986. Is the embryo of Nymphaealean plants (Nymphaeales s.l.) dicotyledonous? Phytomorphology 46: 171–190.
Tomlinson PB. 2016. The botany of mangroves. Cambridge, UK: Cambridge University Press.
Vollbrecht E, Reiser L, Hake S. 2000. Shoot meristem size is dependent on inbred background and presence of the maize homeobox gene, knotted1. Development 127: 3161–3172.
Weatherwax P. 1920. Position of scutellum and homology of coleoptile in maize. Botanical Gazette 69: 179–182.
Wu H, Zhang R, Scanlon MJ. 2024. A multiplexed transcriptomic analysis of a plant embryonic hourglass. BioRxiv. doi: 10.1101/2024.04.04.588207.