Origin and evolution of apical growth in higher plants

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Abstract

The article is devoted to the analysis of the structure, putative function and molecular genetic regulation of the apical meristems in gametophytes and sporophytes of higher plants within the framework of the question about the origin and evolution of their apical growth. The presence of several AIs and secondary plasmodesmata in the apical meristems of gametophytes of Anthocerotophyta and Marchantiophyta and in the sporophytes of Lycopodiales and Isoetales (Lycopodiopsida) indicates that the mechanism of post-cytokinetic plasmodesmata formation that enabled the evolutionary emergence of the simplex apical meristem might have arisen in the last common ancestor of higher plants. The reversion to the monoplex “algal” type of the apical meristem most likely occurred independently in the gametophytes of Bryophyta and the sporophytes of Selaginellales and Polypodiopsida as a consequence of the putative loss of this mechanism. Presence of intercalary zone of proliferating cells in the sporophytes of all bryophytes suggests that a multicellular intercalary meristem was ancestral for the diploid generation of higher plants while the transient apical meristem of the embryo of mosses could have arisen as a result of co-option and modification of the programs regulating the apical meristem of gametophytes. Among the key regulators of apical meristems, only C1KNOX transcription factors (TFs) seem to be sporophyte-specific. Presumably, they have initially regulated the delay of meiosis and diffuse cell proliferation of the ancestral multicellular sporophyte. Whereat they could control the newly evolved intercalary meristem, and the subsequent shift of their expression to the apical pole of the embryo played a key role in the emergence of the apical meristem in sporophytes. Although homologs of WOX transcription factors in bryophytes belong to the T1 superclade that is most distantly related to the T3 (or WUS) superclade of key regulators of the shoot apical meristem of angiosperms, they regulated the apical meristem in gametophytes of liverworts as their counterparts from T3 clade. Expression of WOX homologues, that are phylogenetically more close to WUS, in leaf primordia of lycophytes and root primordia of ferns suggests that the ancestral role of these TFs in sporophytes was the control of organ initiation. Presumably the role of the organizer of the apical meristem arose only in the WUS/WOX5 clade of the T3WOX superclade. Contradictory data on expression of WOX homologs in different gymnosperms do no allow to judge whether members of WUS/WOX5 clade already gained the function of the “organizer” of the shoot apical meristem in the common ancestor of seed plants or only in angiosperms. As the components of the CLE/CLAVATA module are present in the genomes and transcriptomes of the gametophytes of bryophytes and sporophytes of lycophytes, ferns and seed plants, most likely this regulatory module has evolved in the common ancestor of higher plants. Components of this module are shown to have similar functions in the regulation of apical meristems in bryophytes and angiosperms. However they have significant difference between two groups: in the latter CLE/CLAVATA module maintains the apical meristem through a feedback loop with WUS TF, while in the former this module does not interact with WOX homologs. Presence of at least two out of four of regulators of leaf development (ARP, C3HDZ, YABBY and KANADI) in hornworts, liverworts and mosses and presence of all four regulators in all bryoophytes together suggests that they all were already present in the last common ancestor of land plants. These data also indicate that the apical meristems of bryophyte gametophytes have already evolved the regulatory prerequisites for organogenesis. In sporophytes of lycophytes and ferns all the above mentioned regulators are expressed not only in primordia of lateral organs, but also in the shoot apical meristem. Together with the fact that lycophytes and some ferns have dichotomous branching, these data suggest that the program of lateral organs formation in the apical meristem could have evolved as a result of modification of the shoot dichotomy program. Presumably, the functional specificity of the same regulators in different taxa reflects the differences in the distribution and putative action of phytohormone auxin.

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About the authors

M. A. Romanova

St. Petersburg State University

Author for correspondence.
Email: m.romanova@spbu.ru
Russian Federation, St. Petersburg

V. V. Domashkina

St. Petersburg State University; Komarov Botanical Institute RAS

Email: m.romanova@spbu.ru
Russian Federation, St. Petersburg; St. Petersburg

A. I. Maksimova

Komarov Botanical Institute RAS

Email: m.romanova@spbu.ru
Russian Federation, St. Petersburg

O. V. Voitsekhovskaja

Komarov Botanical Institute RAS

Email: m.romanova@spbu.ru
Russian Federation, St. Petersburg

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2. Fig. 1. Phylogenetic tree for higher plants and their structural and regulatory innovations. Placement of taxa is based on: Charophyta — Harrison, Morris (2018); bryophytes — Harris et al. (2022); pteridophytes — PPG I (2016); gymnosperms — Yang et al. (2022). Legend: “+” — presence, “–” — absence, “?” — no data, gmtph — gametophyte, sprph — sporophyte. For genes encoding WOX TFs, the affiliation to superclades or clades that are closest to the “organizer” of the apical meristem of flowering plants WUS is indicated. In each taxon, except for bryophytes, there are also representatives of the superclades more distant from WUS.

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3. Fig. 2. Structure and regulation in the apical meristem of seed plants. Schematics of longitudinal sections of the apical meristem of sporophytes of Magnoliidae (A); Gnetidae (B), Pinidae (C). The allocation of zones is based on: Esau (1969), Steeves, Sussex (1989), Gifford, Foster (1989), Tsukaya (2021). Mapping of gene expression and auxin distribution is based on: angiosperms — Nakata et al. (2012), Nardmann, Werr (2013), Shi, Vernoux (2019); gymnosperms — Nardmann et al. (2009), Nardmann, Werr (2013), Finet et al. (2016), Wan et al. (2018), Bueno et al. (2021). AI / AIs — apical initial or initials; OC — organizing center; СМС — central mother cell zone; CZ — central zone; PZ — peripheral zone; P0—P3 — successive stages of development of leaf primordia and leaves; RM — rib meristem. Putative interactions between apical meristem regulators: arrows indicate positive regulation, bars indicate negative regulation. The apical initial or initials of the apical meristem and leaves are shown in different shades of pink, the organizing center and the central mother cell zone are in light brown, the outer tunica layer is shown as rectangles, the cells of the rib meristem are shown as dots, and the sites of auxin synthesis and basipetal transport are shown in green. Solid arrows indicate that information about the synthesis site and transport pathways of auxin is based on their visualization, and dotted lines indicate that they are based on indirect data. For the other captions and symbols see Fig. 1.

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4. Fig. 3. Structure and regulation in the apical meristem of non-seed plants. Schematics of longitudinal sections of the apical meristem of fern sporophytes: Polypodiopsida (A), Equisetopsida (B); schematic of the Polypodiopsida gametophyte and its apical meristem (C); schematics of the apical meristem of lycophyte sporophytes: Selaginellales (D), Lycopodiales (E). The allocation of zones is based on: Stevenson (1976), Paolillo (1963), Romanova et al. (2010), Evkaikina et al. (2017), Romanova et al. (2022). Mapping of gene expression and auxin distribution is based on: ferns — Bharathan et al. (2002), Harrison et al. (2005), Sano et al. (2005), Nardmann, Werr (2012), Ambrose, Vasco (2016), Vasco et al. (2016), Zumajo-Cardona et al. (2019), Vasco, Ambrose (2020); lycophytes — Evkaikina et al. (2017), Spencer et al. (2021), Vasco et al. (2016). LAI / LAIs — leaf apical initial / initials; SI — surface initials; SSI — subsurface initials; CuZ — cup-zone; RAI — root apical initial; sp — spore; rz — rhizoid. SI are marked in pale pink, SSI are in light brown; dots indicate cells of the rib meristem and parenchymatous ridges around the AI in gametophyte. For the other captions and symbols see Figs. 1, 2.

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5. Fig. 4. Structure and regulation of bryophyte meristems. Schematics of gametophytes and longitudinal sections of the apical meristems in Anthocerotophyta (A), Marchantiophyta (B); Bryophyta: protonema (C); gametophores (D) and schematics of sporophytes of Anthocerotophyta (E), Marchantiophyta (F), Bryophyta (G). Mapping of gene expression and auxin distribution is based on: Sakakibara et al. (2014), Yip et al. (2016), Youngstrom et al. (2019), Dierschke et al. (2021), Kochi et al. (2021), Fouracre, Harrison (2022), Nemec-Venza et al. (2022), Frangedakis et al. (2023). ptn — protonema, cln — caulonema, st — seta, ft — foot, im — intercalary meristem. For the other captions and symbols see Figs. 1–3.

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