The evolutionary trajectory of root stem cells
Hans Motte1,2, Boris Parizot1,2, Tao Fang1,2, Tom Beeckman1,2,*
1Ghent University, Department of Plant Biotechnology and Bioinformatics, 9052 Ghent, Belgium
2VIB Center for Plant Systems Biology, 9052 Ghent, Belgium
* Corresponding author: [email protected]
Summary
Root stem cells are crucial for the establishment of roots and are therefore a major evolutionary innovation that enabled land plants to spread on land. Despite their importance, not too much is known about the origin and the molecular players installing and maintaining them. Although still fragmentary, the recent availability of new data for early land plants can be used to identify and analyze the conservation of key regulators of root meristems. In this review, we evaluate the possible conservation of important root stem cell regulators to suggest pathways that might have been important at the origin of roots.
Introduction
About 470 mya, in the Ordovocian period, descendants of the streptophyte algae started to escape gradually from their freshwater environment and conquered step by step a new territory: land [1]. The earliest diverged land plants, bryophytes, were and still are dependent on humid environments as they lack organs to retrieve water from a wider environment. The successful colonization of land therefore mainly came within reach thanks to the roots, which first evolved in lycophytes, and later in ferns and seed plants (Figure 1). Roots not only granted plants with a more efficient foraging of water and nutrients, but also provided anchorage to allow growth in height. During early root evolution, a new meristem originated, including stem cells maintaining a pluripotent cell fate and as such allowing indeterminate growth and the generation of different cell types.
The current knowledge about the control of root stem cells and meristems in early diverged land plants is, however, very limited. Lately, genomics and molecular genetics approaches have become available in these species and are generating promising new data, giving us the opportunity to investigate the role of known pathways. In Arabidopsis, it is clearly demonstrated that root stem cell induction and
maintenance are predominantly controlled by the plant hormone auxin and by WUSCHEL-RELATED HOMEOBOX (WOX), SCARECROW (SCR) and PLETHORA (PLT) transcription factors [2-9]. As root stem cells seem not to be induced by auxin in early diverged land plants [10,11], we will focus in this review on the possible involvement of WOX-, SCR- and PLT-related pathways in a, at least partially, common mechanism in root stem cell determination.
Earlier diverged plants have a less complex root meristem with a considerably lower number of stem cells.
In the root meristem of angiosperms different stem cell types assure the indeterminate growth of the root. In the Arabidopsis root, stem cells surround the quiescent center (QC) that controls their undifferentiated state. Different stem cells give rise to daughter cells with distinct cell fates, respectively: columella root cap; vasculature and ground tissue; lateral root cap and epidermis (Figure 2) [2] .
In earlier diverged plants, the root meristem is less complex. Both in ferns and Selaginellales, the most studied clade within the lycophytes, one supposedly tetrahedral root apical or initial cell is the source of all cells in the root. Cells cut off at the three proximal sides or at the distal side produce the main root or the root cap, respectively (Figure 1) [12-17]. Likewise, the way of root branching seems to have increased in complexity during evolution: lycophyte roots branch dichotomously after installation of an extra initial cell in the root tip; leptosporangiate ferns develop lateral roots after the specification of particular endodermal cells as root apical founder cells; and seed plants require a tightly regulated series of cell divisions from a pluripotent cell file to assure the development of lateral roots (Figure 1) [recently reviewed in 17].
Knowledge on the control of stem cells is, even in Arabidopsis, still limited. However, a few transcription factors have been identified to play key roles in the stem cell regulatory pathways (Figure 2). For example, WOX5 represses the differentiation factor CYCLING DOF FACTOR4 (CDF4) both in the QC and, after movement of the WOX5 protein, also in the columella stem cells [6]. WOX5 is in the QC induced by transcription factor complexes of SCR, PLT and teosinte-branched cycloidea PCNA (TCP) [18]. The SCR and SHORTROOT (SHR) protein are both present in the cortex/endodermal initials. These transcription factor complexes inactivate RETINOBLASTOMA- RELATED (RBR) via a complex auxin- and cyclin-dependent pathway to retain stem cell fate [4].
Additionally, PLTs, forming a gradient with an expression maximum in the stem cell niche, target a vast number of genes to repress differentiation [19,20] and are required to maintain stem cell fate as well [9]. For further reading on the regulation of root stem cells, we refer to other reviews [7,21,22].
Due to the less complex organization of root meristems of ferns and Selaginellales, a more elementary molecular organization of the root stem cells and meristems can be presumed in these species. The study of the pathways controlling root stem cells in early diverged land plants can therefore guide us to the minimal, or possibly alternative, molecular players that are required to install and maintain stem cell fate, and by extension to a deeper understanding of pluripotency and organogenesis competence.
Of important note is that lycophyte roots originated independently from roots of ferns and seed plants (Figure 1) [23]. Still, there has been a strong convergent evolution, possibly due to the presence of a rudimentary root developmental program in a common ancestor [24]. This is reflected in the remarkable similar morphology of the roots from the different clades, all including typical root features such as a root cap, root hairs and an endodermis.
Omics and molecular tools in early diverged rooting land plants
At present, there are hardly any reports on the genetic and molecular regulation of roots in early diverged land plants, partially due to a lack of data and molecular tools. To our knowledge, there are for instance only four lycophyte genomes [25-28], all belonging to the Selaginellales and two fern genomes available [29].
The lack of non-seed plant genomes is addressed by initiatives like the 1KP project, that sequenced the transcriptomes of about 1000 diverse plants to have at least an idea on the coding sequences and their evolution in the plant kingdom [30]. This allowed for more extensive evolutionary studies, as illustrated for the AINTUGEMENTA (ANT) gene family (see below)[31].
In addition to the 1KP project, the 10KP project is currently sequencing 10 000 plant genomes to obtain a reference genome for each plant genus within the plant kingdom, including at least 1000 non- seed land plant genera [32].
The current lack of genome sequences also obstructs the use of lycophytes or ferns in genome wide expression analyses, for which most studies do not focus on roots (Table 1), and which hence limits the data mining resources for these two pivotal clades with respect to root evolution.. At least the study by L Huang and J Schiefelbein [24], who compared the root meristem zone with the elongation zone, provides a useful resource to identify genes associated to the root meristem.
For now, studies to test the evolutionary conservation of root meristem genes included comparisons of hormonal effects, complementation assays, expression studies or transcriptome comparisons [recently reviewed in 33]. In order to effectively validate putative evolutionary conserved genes, there is still a need for good (molecular-genetic) tools. So far, some fern species can be transformed [34-36], chemically or radioactively mutagenized [37] or mutagenized in a targeted way via gene silencing [38]. Recently, transient transfection of Selaginella moellendorffii protoplasts was established, and enables limited validation of for example conserved transcriptional responses. As such, using the
auxin responsive DR5 reporter, a conserved auxin signaling pathway was experimentally confirmed [39]. Such techniques are promising, but an expansion of the molecular toolbox as is present for other model plants, and which would facilitate evolutionary studies, awaits more intensive use of these techniques in lycophytes and ferns.
Different WUSCHEL-RELATED HOMEOBOX members might control stem cells via distinct mechanisms
The WOX family has different subclades, including the modern WOX-clade that contains the root stem cell regulator WOX5 but which is restricted to seed plants and ferns, and more ancient subclades to which the lycophyte WOX members belong [recently reviewed by 40]. Interestingly, the ancient homologues lack a canonical WUS-box that is essential for their transcriptional repressive activity [41,42] and essential for stem cell and quiescent center control in seed plants. If WOX transcription factors are involved in the lycophyte root stem cell fate, they might work as transcriptional activators and hence follow a different mechanism. Interestingly, multiple Selaginella moellendorffii WOX homologues are more highly expressed in the root meristem [24] and WOX homologues in the moss Physcomitrella patens contribute to stem cell formation [43]. This supports the idea of an involvement of the ancient members in stem cell determination and could indicate that lycophytes adopted a pathway from their common ancestor with the bryophytes to enable root stem cell initiation. Such ancient WOX homologues are moreover associated with the asymmetrical divisions that lead to a new root initial stem cell in the fern Ceratopteris richardii [44]. Even in Arabidopsis such mechanism might still be present: WOX13, a representative of the ancient clade, is expressed in the root meristem, seemingly in or near the QC [43]. Moreover, WOX13 together with WOX14, another ancient WOX gene in Arabidopsis, are strongly differentially expressed during lateral root formation and the establishment of a new root meristem [45]. A putative role of WOX13 in stem cell fate control could however not be validated [43].
The absence of WOX5 orthologues in lycophytes further corroborates the independent origin of roots in this clade. In seed plants and ferns a homologous WOX5-orthologue dependent pathway functions in the shoot [5,46-49], which suggests that in these clades roots evolved from shoots or recruited the shoot genetic program. Because this evolution was dependent on the availability of the modern WOX- clade, it is likely that roots originated in a common ancestor of ferns and seed plants after their divergence from the lycophytes.
The fern Ceratopteris richardii has a WOX5 ortholog, CrWUL , but its root meristem does not have a quiescent center and shows a completely different cell division pattern compared to seed plants (Figure 1) [13,17]. Additionally, in contrast to WOX5, CrWUL is not able to move from cell to cell [50], and is not associated with the root apical stem cell itself [44]. On the other hand, the CrWUL can still functionally complement Arabidopsis wox5 mutants [50] and hence is part of a conserved
pathway. Overall, these observations show that ferns adopted a common pathway in a different way to develop roots, and supports the possibility that fern roots have an independent origin as well.
In conclusion, the WOX5-mediated control of stem cell determination is clearly not a conserved mechanism within all land plants. It arose in ferns, but despite its functional conservation, the different root meristem organization and expression domain of the WOX5 orthologue of ferns suggests a different control of stem cell proliferation. More ancient members of the WOX family might have possible roles in stem cell determination as well, but act probably through different mechanisms.
Possible conserved control of PLETHORAs by WOX transcription factors
PLTs belong to the AINTEGUMENTA (ANT) and ANT-LIKE (AIL) transcription factor family and are part of the euANT/AIL subclade [reviewed by 51]. In particular PLT1, PLT2, PLT3 and PLT4/BABYBOOM (BBM) are known and important regulators of the root stem cells [8,9], but diversification of the different PLTs only occurred during seed plant evolution. Ferns contain orthologues of both ANT and AIL, whereas lycophytes (and also bryophytes) only have homologs in an ANT/AIL sister clade [31]. Still, motifs between lycophyte ANT/AIL homologues and PLTs are highly conserved (Figure 3A), supportive for a conserved function. Interestingly, regulatory elements in the promoter sequences of AIL genes are relatively well conserved within all land plants [31], further indicating their possible involvement in conserved, stem cell controlling pathways. Indeed, even in the moss Physcomitrella patens, the four AIL homologues APB1-4 (for ANT, PLT, BBM) were shown to determine stem cell identity [52]. Likewise, overexpression of the CrANT in C.
richardii results in increased regeneration capacity [53], further supporting a role in stem cell control.
Remarkably, the regulatory regions of AIL genes throughout all land plants contain WOX DNA- binding motifs, suggesting a conserved control by WOX transcription factors [31]. Despite the functional diversification of the WOX family through evolution (see above), the WOX-dependent transcriptional regulation of PLT-like genes seems to have been conserved. Such control has previously been suggested to occur in the distal stem cells in the root meristem of Arabidopsis [54], but awaits functional validation.
SCARECROW and RETINOBLASTOMA-RELATED interactions were present at the origin of roots
In contrast to the WOX and the ANT/AIL family, for which some functional or expression studies are available, there is not much known about the possible roles of SCR-like transcription factors in the root of early diverged land plants. However, in angiosperms, SCR has been characterized, together with its dimerizing partner SHORTROOT (SHR), as a key factor in stem cell control. SCR and SHR are both highly conserved within land plants and were established prior to divergence of the most early land plants [55]. Interestingly, the stem cell control by SCR depends on its interaction with RETINOBLASTOMA-RELATED (RBR), an even more conserved protein and homolog of the
human tumor suppressor pRb [4]. Both pRb and RBR are involved in stem cell function and contain LxCxE-binding sites, showing a cross-kingdom conservation [56 and refs therein]. Interestingly, the LxCxE motif is also conserved in SCR homologues in all land plants (Figure 3B) and essential for its interaction with RBR [4,57]. Their common appearance in land plants argues for their potential participation to the earliest mechanisms in (root) stem cell determination. Moreover, SCR, SHR and RBR orthologues show an enriched representation in Selaginella moellendorffii root meristems [24]
and are associated to certain stem cell types in the moss Physcomitrella patens [58,59], suggesting that plants might have made use of these ancient factors to generate root meristems. The elucidation of their role in root-bearing spore plants awaits further investigation.
Conclusions
Our modern seed plants can produce heavily branching extensive root systems supporting their growth on dry land conditions. However, going back in time and investigating roots of representatives of earlier diverged plant groups learns that this has not always been the case. Roots seem to have gradually or step-wisely evolved to the highly efficient uptake organs that we know from seed plants.
At the structural level, root meristems became more complex with a division of tasks among multiple stem cells instead of having only one single apical stem cells. Furthermore, stem cell niches outside the apical meristem arose both in the ferns and the seed plants enabling lateral branching. At the molecular level, stem cell activity and maintenance is dominated by the plant hormone auxin in seed plants whereas this seems to not be the case for ferns and lycophytes. Although functional data is as good as missing for the early diverging groups, PLT, SHR/SCR-RBR and WOX pathways seem to be conserved in all groups, but, as is the case for the WOX pathway, probably have been utilized in alternative ways to create roots. Remarkably, roots originated at least twice and there are several examples both at the structural as at the molecular level of convergent evolution. The advent of an increasing number of genome sequences combined with the increased interest of developmental biologists for a broader range of model species promises to prelude an exciting era in root developmental biology.
Acknowledgements
We thank Maria Fransiska Njo for help with artwork. Work in the Beeckman lab was supported by grants G002817N [Bilateral Research Cooperation with the Chinese Ministry of Science and Technology (MOST) 2016YFE0109900], G022516N, G020918N, and G024118N from the Research Foundation-Flanders (FWO).
Figures
Figure 1: Overview of the evolution of root meristem patterning and root branching mechanisms in different land plant lineages. The apical cell, quiescent center or lateral root primordium is indicated in yellow. In seed plants, different types of stem cells give rise to distinct cell types. In lycophytes and ferns, only one initial provides all different cell types for the root. Lateral root formation requires in seed plants a tight control of a series of cell divisions. In leptosporangiate ferns, this occurs by recruiting specific endodermal cells as precursor cells for new apical cells. In lycophytes, not capable of forming lateral roots, dichotomous root branching occurs by the installation of a new apical cell in the root meristem. * indicate independent origins of roots. It is so far not clear whether the roots of ferns and seed plants originated from one common ancestor or evolved independently, as indicated in gray.
Figure 2: The Arabidopsis root meristem and control of stem cell maintenance. The stem cell niche is composed out of a QC surrounded by different stem cells or initials. WOX5, SCR and PLTs are predominant transcription factors controlling stem cell maintenance or differentiation. SCR- and PLT- dependent WOX5 suppresses differentiation in the QC and columella stem cells. SCR-SHR complexes induces together with high auxin levels stem cell fate in the cortex/endodermal initials.
Figure 3: Indications of the functional conservation of main regulators of root stem cells. (A) Motifs and domains of different ANT/AIL family members. The APETALA2 binding domain and the euANT motifs are shown in light-blue and orange, respectively. The other colors indicate different conserved motifs as reported by M Dipp-Álvarez and A Cruz-Ramírez [31]. For Arabidopsis thaliana, the 4 most diverse members are presented and Scaffold 2011839 and Scaffold 2076641 are presented for Lycopodium deuterodensum and Isoetes sp., respectively. The latter have almost all motifs that are present in diverse genes from seed plants, suggesting a possible functional conservation. B) Protein sequence of SCARECROW homologues in diverse land plants. All homologues have the LxCxE motif (indicated in gray by the black arrows) which allows for interaction with the highly conserved stem cell and differentiation factor RBR. The presented proteins are encoded by AT3G54220 (Arabidopsis thaliana), LOC_Os11g03110 (Oryza sativa), PAB00028774 (Picea abies), ATR1127G062 (Amborella trichopoda), onekp VIBO_scaffold_2075755 (Osmunda javanica), onekp CVEG_scaffold_2001983 (Azolla caroliniana), SMO351G0478 (Selaginella moellendorffii), Mapoly0014s0183 (Marchantia polymorpha) and Pp3c19_18560 (Physcomitrella patens).
Table1: Lycophyte and fern genome-wide gene expression studies.
Clade Species Assembly Samples Reference
Lycophyte Selaginella moellendorffii Genomic Shoot meristem subdomains and microphyl primordium
[60]
Lycophyte Selaginella moellendorffii Genomic Root meristematic and non-meristematic region
[24]
Lycophyte Selaginella moellendorffii Genomic Microphyl, stem and root tissue [61]
Lycophyte Selaginella moellendorffii Genomic Root, shoot and rhizophore tips and microphyls
[39]
Lycophyte Selaginella moellendorffii Genomic Plants under different hydration conditions [27]
Lycophyte Selaginella tamariscina Genomic Plants under different hydration conditions [27]
Lycophyte Selaginella lepidophylla Genomic Microphyls from plants under different
hydration conditions [28]
Lycophyte Selaginella bryopteris De novo Frond and root tissue [62]
Lycophyte Selaginella uncinata De novo Blue and red microphyls [63]
Lycophyte Isoetes Sinensis De novo Microphyls from plants under terrestrial or submerged condition
[64,65]
Fern Azolla filiculoides De novo Root meristems of plants treated with auxin or cytokinin
[66]
Fern Ceratopteris richardii De novo Male and hermaphrodite gametophytes [67]
Fern Equisetum arvense De novo Shoot meristem subdomains and leaf primordium
[60]
Fern Lygodium japonicum De novo Different tissues throughout the life cycle [68]
Fern Polypodium amorphum De novo Sporophyte leaf tissue and gametophytes [69]
Fern Vandenboschia speciosa De novo Sporophytes and gametophytes [70]
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