Lycopodium root meristem dynamics supports homology between shoots and roots in lycophytes

Abstract

Roots have played a pivotal role in the conquest of land by vascular plants, yet their origin has remained enigmatic. Palaeobotanical evidence suggests that roots may have originated from subterranean shoots in some lycophyte species. If this hypothesis is correct, it would follow that the roots and shoots of extant lycophytes share fundamental developmental mechanisms. We tracked meristem dynamics in root and shoot apices of Lycopodium clavatum using a thymidine analogue and expression patterns of histone H4, respectively. Then we compared the meristem dynamics of roots and shoots to identify developmental similarities. Both apical meristems contained a quiescent tissue characterised by a low frequency of cell division. Actively dividing cells appeared in the quiescent tissue during dichotomous branching of both roots and shoots. As a result, the parental meristem divides into two daughter meristems, which give rise to new root or shoot apices. These striking similarities in meristem dynamics provide new neobotanical data that support the shoot-origin hypothesis of lycophyte roots. Although Lycopodium roots may have originated from subterranean shoots of Devonian lycophytes, these shoots may have changed into root-bearing axes in other extant lycophyte lineages.

An evidence-based 3D reconstruction of Asteroxylon mackiei, the most complex plant preserved from the Rhynie chert

“…Our new reconstruction indicates that rooting axes connected to root-bearing axes at anisotomous branch points. Based on development of extant lycopsids ( Bierhorst, 1971 ; Fujinami et al, 2021 ; Gola, 2014 ; Guttenberg, 1966 ; Harrison et al, 2007 ; Hetherington and Dolan, 2017 ; Imaichi, 2008 ; Imaichi and Kato, 1989 ; Ogura, 1972 ; Ollgaard, 1979 ; Spencer et al, 2021 ; Yi and Kato, 2001 ; Yin and Meicenheimer, 2017 ), there are two modes of branching that could produce anisotomous branch point morphology, endogenous branching, or dichotomous branching. Endogenous branching is the mode of branching where the meristem of the new axis develops from the internal tissues of the parent axis and breaks through the parent tissue to emerge, a mode of development typical of the initiation of roots of extant lycopsid species.…”

“…In extant lycopsids, roots originate endogenously from shoots or specialised root producing structures, such as rhizophores ( Figure 6 ). Once developed, roots, shoots, and rhizophores branch dichotomously ( Chomicki et al, 2017 ; Fujinami et al, 2021 ; Gola, 2014 ; Harrison et al, 2007 ; Hetherington and Dolan, 2017 ; Imaichi, 2008 ; Imaichi and Kato, 1991 ; Ollgaard, 1979 ; Yin and Meicenheimer, 2017 ). However, the two daughter axes produced by dichotomous branching are always identical to the original axis: a shoot axis may branch dichotomously to form two identical shoot axes, a root axis may branch to form two identical root axes, and a rhizophore branches to form two identical rhizophores ( Chomicki et al, 2017 ; Fujinami et al, 2021 ; Gola, 2014 ; Harrison et al, 2007 ; Hetherington and Dolan, 2017 ; Imaichi, 2008 ; Imaichi and Kato, 1991 ; Ollgaard, 1979 ; Yin and Meicenheimer, 2017 ).…”

An evidence-based 3D reconstruction of Asteroxylon mackiei the most complex plant preserved from the Rhynie chert

“…While branching evidence in our reconstruction is consistent with the development of rooting axes from root-bearing axes by dichotomy, we tested if there was evidence for endogenous development because roots originate endogenously in extant lycopsids (Bierhorst, 1971;Bruchmann, 1874;Fujinami et al, 2020;Guttenberg, 1966;Hetherington and Dolan, 2017;Imaichi, 2008;Imaichi and Kato, 1989;Ogura, 1972;Øllgaard, 1979;Wigglesworth, 1907;Yi and Kato, 2001). Therefore, we searched for meristems of rooting axes preserved soon after they originated from root-bearing axes.…”

“…Our new reconstruction indicates that rooting axes connected to root-bearing axes at anisotomous branch points. Based on development of extant lycopsids (Bierhorst, 1971;Fujinami et al, 2020;Gola, 2014;Guttenberg, 1966;Harrison et al, 2007;Hetherington and Dolan, 2017;Imaichi, 2008;Imaichi and Kato, 1989;Ogura, 1972;Øllgaard, 1979;Spencer et al, 2020;Yi and Kato, 2001;Yin and Meicenheimer, 2017) there are two modes of branching that could produce anisotomous branch point morphology, endogenous branching or dichotomous branching. Endogenous branching is the mode of branching where the meristem of the new axis develops from the internal tissues of the parent axis and breaks through the parent tissue to emerge, a mode of development typical of the initiation of roots of extant lycopsid species (Bierhorst, 1971;Bruchmann, 1874;Fujinami et al, 2020;Guttenberg, 1966;Hetherington and Dolan, 2017;Imaichi, 2008;Imaichi and Kato, 1989;Ogura, 1972;Øllgaard, 1979;Wigglesworth, 1907;Yi and Kato, 2001).…”

“…Based on development of extant lycopsids (Bierhorst, 1971;Fujinami et al, 2020;Gola, 2014;Guttenberg, 1966;Harrison et al, 2007;Hetherington and Dolan, 2017;Imaichi, 2008;Imaichi and Kato, 1989;Ogura, 1972;Øllgaard, 1979;Spencer et al, 2020;Yi and Kato, 2001;Yin and Meicenheimer, 2017) there are two modes of branching that could produce anisotomous branch point morphology, endogenous branching or dichotomous branching. Endogenous branching is the mode of branching where the meristem of the new axis develops from the internal tissues of the parent axis and breaks through the parent tissue to emerge, a mode of development typical of the initiation of roots of extant lycopsid species (Bierhorst, 1971;Bruchmann, 1874;Fujinami et al, 2020;Guttenberg, 1966;Hetherington and Dolan, 2017;Imaichi, 2008;Imaichi and Kato, 1989;Ogura, 1972;Øllgaard, 1979;Wigglesworth, 1907;Yi and Kato, 2001). Dichotomous branching is the mode of branching where the parent meristem splits in two to produce two daughter axes, a mode of development typical of roots, shoots and rhizophores in extant lycopsids (Bierhorst, 1971;Bruchmann, 1874;Gola, 2014;Guttenberg, 1966;Harrison et al, 2007;Hetherington and Dolan, 2017;Imaichi, 2008;Imaichi and Kato, 1989;Ogura, 1972;Øllgaard, 1979;Spencer et al, 2020;Wigglesworth, 1907;...…”