Annals of Botany 110: 205 –212, 2012
doi:10.1093/aob/mcs136, available online at www.aob.oxfordjournals.org
REVIEW: PART OF A SPECIAL ISSUE ON ROOT BIOLOGY
The evolution of root hairs and rhizoids
Victor A.S. Jones and Liam Dolan *
Department of Plant Sciences, University of Oxford, Oxford OX1 3RB, UK
* For correspondence. E-mail [email protected]
Received: 15 March 2012 Returned for revision: 1 May 2012 Accepted: 28 May 2012 Published electronically: 23 June 2012
† Background Almost all land plants develop tip-growing filamentous cells at the interface between the plant and
substrate (the soil). Root hairs form on the surface of roots of sporophytes (the multicellular diploid phase of the
life cycle) in vascular plants. Rhizoids develop on the free-living gametophytes of vascular and non-vascular
plants and on both gametophytes and sporophytes of the extinct rhyniophytes. Extant lycophytes (clubmosses
and quillworts) and monilophytes (ferns and horsetails) develop both free-living gametophytes and free-living
sporophytes. These gametophytes and sporophytes grow in close contact with the soil and develop rhizoids
and root hairs, respectively.
† Scope Here we review the development and function of rhizoids and root hairs in extant groups of land plants.
Root hairs are important for the uptake of nutrients with limited mobility in the soil such as phosphate. Rhizoids
have a variety of functions including water transport and adhesion to surfaces in some mosses and liverworts.
† Conclusions A similar gene regulatory network controls the development of rhizoids in moss gametophytes and
root hairs on the roots of vascular plant sporophytes. It is likely that this gene regulatory network first operated in
the gametophyte of the earliest land plants. We propose that later it functioned in sporophytes as the diploid phase
evolved a free-living habit and developed an interface with the soil. This transference of gene function from gametophyte to sporophyte could provide a mechanism that, at least in part, explains the increase in morphological
diversity of sporophytes that occurred during the radiation of land plants in the Devonian Period.
Key words: Rhizoids, root hairs, Physcomitrella patens, Arabidopsis thaliana, root, root systems, nutrient
uptake, soil, tip growth, life cycle, alternation of generations, streptophyte.
IN T RO DU C T IO N
The emergence of the first land plants sometime before 470
million years ago was a pivotal event in Earth history, which
had far-reaching effects on the atmosphere and climate, and
made possible subsequent invasions of the land by animals
and the establishment of complex terrestrial ecosystems
(Berner, 1997; Bateman et al., 1998). Land plants evolved
from streptophyte algae, and a number of innovations were
involved in their adaptation to terrestrial life. Among these
was the evolution of rooting systems for anchorage, water
uptake and nutrient acquisition, which was a key step that
allowed the spread of plants on dry land (Bateman et al.,
1998; Raven and Edwards, 2001). Others included the elaboration of meristems and complex tissue systems leading to the
formation of complex land plant body plans; the evolution of
desiccation tolerance, which allowed plants to survive life in
the air; and ultimately the evolution of water transport
systems, which allowed plants to move water from soil stores
to the tops of tall trees. The appearance of land plants also
had major impacts on geochemical cycles. Through the physical action of roots and the secretion of acids into the rhizosphere, plants greatly accelerated the weathering of silicate
minerals. This increase in the rate of the reaction of atmospheric CO2 with calcium and magnesium silicates caused a shift in
the equilibrium of the long-term carbon cycle and drastically
reduced atmospheric CO2 levels, causing global climate
cooling (Berner, 1997; Raven and Edwards, 2001; Lenton
et al., 2012).
Filamentous cells develop at the interface between almost
all land plants and the substrate in which they grow at some
stage during the plant’s life cycle. Root hairs form on the
root surface of sporophytes (the multicellular diploid phase
of the life cycle) in vascular plants. Rhizoids develop on the
free-living gametophytes (the multicellular haploid phase of
the life cycle) of extant vascular and non-vascular plants and
on both the gametophytes and rootless sporophytes of extinct
rhyniophytes. Extant lycophytes and monilophytes develop
both free-living gametophytes and free-living sporophytes.
These gametophytes and sporophytes grow in close contact
with the substrate and develop rhizoids and root hairs, respectively. Both rhizoids and root hairs elongate by tip growth
(Carol and Dolan, 2002; Pressel et al., 2008). During tip
growth, growth is restricted to a small area at the apex of the
elongating cell. This contrasts with the diffuse growth
typical of most cell types in plants, in which growth occurs
over more extensive areas of the cell surface.
This review outlines the diversity of filamentous, tip-growing
cells that interface with the substrate of land plants and their
aquatic ancestors. The literature describing their function and the
genetic mechanisms that control their development is reviewed.
P H Y LO G E N E T I C RE L AT I O N S H I P S A M O N G
L A N D P L A N T S A N D RE L AT E D S T R E P TO P H Y T E
A L GA E
Land plants and the streptophyte algae (Charales, Coleochaetales,
Zygnematales, Klebsormidiales, Chlorokybales and Mesostigma)
# The Author 2012. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved.
For Permissions, please email: [email protected]
206
Jones & Dolan — Evolution of root hairs and rhizoids
together constitute a monophyletic group called the streptophytes. Streptophyte algae are a paraphyletic group, in that
they do not include all descendants of a single common ancestor, while the land plants are monophyletic (include all descendants of a single common ancestor). It is unclear which
algal group is most closely related to the land plants. It is
likely that one of three groups, Coleochaetales, Charales or
Zygnematales, is sister to the land plants. Further phylogenetic
analyses are needed to define unequivocally the closest algal
relative of the land plants (see, for example, Karol et al.,
2001; Qiu et al., 2006; Finet et al., 2010; Wodniok et al.,
2011; Leliaert et al., 2012) (Fig. 1). Three early diverging
clades of land plants, liverworts, mosses and hornworts, are
generally held to constitute a paraphyletic grade known as
the bryophytes, though some recent molecular phylogenies
do resolve the bryophytes as a monophyletic group (for
example Finet et al., 2010). There is evidence that the earliest
land plants had affinities to extant liverworts, and that liverworts are the earliest diverging land plant lineage (references
in Kenrick and Crane, 1997a; Karol et al., 2001; Wellman
et al., 2003; Qiu et al., 2006, 2007; Rubinstein et al., 2010).
The vascular plants, which develop water-conducting tissues
made up of cells with thickened lignified walls (xylem), are
a monophyletic group that includes the lycophytes, the monilophytes (ferns and horsetails) and the seed plants (Kenrick
and Crane, 1997b; Qiu et al., 2006). These phylogenetic relationships provide an evolutionary framework for understanding the distribution of filamentous cells at the interface
between plant and substrate (Fig. 1).
R HI Z OI DS A ND RO OT H AI RS D E VELO P AT T H E
P L A N T – S U B S T R AT E I N T E R FAC E I N
S T R E P TO P HY T E A L GA E AN D L A ND P L A NT S
Rhizoids develop in the haploid phase of some of the streptophyte algae, such as Chara (Charophytales) and Spirogyra
(Zygnematales), but not in others such as the Coleochaetales
(Lewis and McCourt, 2004). Rhizoids are unicellular in the
Zygnematales and multicellular in the Charales. Rhizoids do
not form in the diploid phase of the life cycle of streptophyte
algae, which is unicellular and consists only of a zygote that
undergoes meiosis. In contrast, the land plant life cycle consists of two distinct multicellular phases, comprising the
diploid sporophyte and the haploid gametophyte. The gametophyte produces gametes that fuse to form a zygote that undergoes mitosis to form the multicellular diploid sporophyte.
In turn, cells of the sporophyte undergo meiosis to form
haploid spores that divide to form multicellular haploid
gametophytes. Life cycles with multicellular haploid and
diploid phases are said to display alternation of generations
(Hofmeister, 1851; Strasburger, 1894; (Kenrick and Crane,
1997a).
In the earliest diverging land plant lineages, the liverworts,
mosses, and hornworts, the gametophyte is the only free-living
stage of the life cycle. As this phase of the life cycle is in direct
contact with the substrate, the gametophyte develops a system
of rhizoids. In contrast, the relatively simple sporophyte is
either entirely (liverworts and mosses) or mostly (hornworts)
nutritionally dependent upon the haploid phase, and does not
make contact with the substrate or develop rhizoids (McManus
and Qiu, 2008). Liverwort and hornwort rhizoids are unicellular,
but those of mosses are multicellular (Crandall-Stotler and
Stotler, 2008; Goffinet et al., 2008; Renzaglia et al., 2008).
In contrast to the bryophytes, vascular plants evolved hairbearing axial organs that anchor the sporophyte and are
involved in the absorption of nutrients and water. These
organs, roots, possess unique defining characteristics including
the formation of a protective root cap at the distal, growing end
of the axes, and endogenous branching, in which lateral roots
are derived from cells in the centre of the root (the pericycle).
This contrasts with shoots where there is no cap and shoot cells
at and near the surface of axes develop into branches (Raven
Root hairs on sporophyte
Rhizoids on gametophyte
Charophytes Liverworts
Mosses
Bryophytes
Hornworts
Lycophytes Monilophytes
Seed Plants
Vascular Plants
F I G . 1. The occurrence of rhizoids and root hairs in extant land plant lineages. Streptophyte algae are the closest relatives of land plants, and some members
possess rhizoids. Rhizoids develop on the gametophytes of some land plants (liverworts, mosses, hornworts, lycophytes and monilophytes). Root hairs are found
only on the roots of the sporophytes of vascular plants. The lycophytes and monilophytes develop both rhizoids on their gametophytes and root hairs on their
sporophytes. Rhizoids are multicellular in the mosses. All other land plants develop unicellular rhizoids and root hairs. Tree after Qiu et al. (2006).
Jones & Dolan — Evolution of root hairs and rhizoids
and Edwards, 2001). Almost all roots develop filamentous
cells (root hairs) along their surface at the plant – soil interface.
These hairs have been shown to be important for nutrient
uptake (discussed in detail below). In some vascular plants,
namely monilophytes and lycophytes, the gametophyte is
still present as a free-living but ephemeral organism and develops rhizoids (Banks, 1999, 2009) (Fig. 1). In contrast, the gametophyte is retained by and parasitic upon the sporophyte in all
seed plants and reduced to a few cells (the pollen grains and
embryo sac) in the angiosperms, where no rhizoids develop.
RO OT S E VOLV E D AT L E A S T T W I C E I N T H E
LAND PLANTS
Fossil evidence indicates that roots had evolved among the
lycophytes by the Early Devonian. For example, Asteroxylon
mackei, found in the 411 million-year-old Rhynie chert, has
simple root-like structures that contrast with the leafy shoot
(Kidston and Lang, 1920; Kenrick and Crane, 1997b). Roots
most probably evolved independently in other vascular plants
from rootless ancestors (Kenrick and Crane, 1997b; Gensel
et al., 2001; Raven and Edwards, 2001); although it has been
argued that roots evolved only once in the vascular plants
(Schneider et al., 2002), this is rebutted by phylogenetic analyses that consider fossil taxa (Friedman et al., 2004). It has
also been suggested that roots evolved twice within the euphyllophyte clade because the orientation of the root axis relative to
A
B
F
the shoot axis is different in the embryos of seed plants and
monilophytes (Gensel and Berry, 2001; Raven and Edwards,
2001). This hypothesis remains to be tested phylogenetically,
and difficulties may arise because of the poor preservation of
this stage of the life cycle in the fossil record. Despite the probable independent evolution of root axes in different groups of
plants, root hairs are found on the roots of the sporophytes of
all major vascular plant lineages (Dittmer, 1949; Pearson,
1969; Banks, 2009) (Fig. 2).
RO OT HA IR S ARE I M PO RTA NT FOR N UT RIE NT
U P TAK E
Most angiosperms form root hairs at some stage during the development of the root system. They may be very short in some
species such as onion (Alium cepa) or much longer in other
species such as members of the Brassicales (reviewed in
Jungk, 2001). Root hairs play a crucial role in the uptake of
essential inorganic nutrients from the soil (Nye, 1966; Föhse
et al., 1991; Gahoonia and Nielsen, 1997, 1998). These essential nutrients are taken up in ionic form from the soil water at
the root surface (Marschner, 2012). As the nutrient is transported into the plant it is replaced at the root surface by diffusion if it is present in sufficient concentrations in the soil water.
Nitrate and ammonium are soluble and diffuse through the soil
water, thereby replenishing the supply of these ions at the root
surface. Phosphate on the other hand is not mobile in the soil
D
C
G
207
E
H
F I G . 2. Rhizoid and root hair morphology in Chara braunii and land plants: (A–E) rhizoids and (F –H) root hairs. (A) Rhizoids of Chara braunii; (B) rhizoids of
the liverwort Marchantia polymorpha gametophyte; (C) multicellular rhizoids on the moss Physcomitrella patens gametophyte; (D) rhizoids of the hornwort
Anthoceros punctatus gametophyte; (E) rhizoids on the gametophyte prothallus of the fern Ceratopteris richardii; (F) root hairs on the root of the
Selaginella kraussiana sporophyte; (G) root hairs on the root of the fern Ceratopteris richardii sporophyte; (H) root hairs of the angiosperm Arabidopsis thaliana
sporophyte. Arrowheads indicate rhizoids or root hairs. Scale bars ¼ 1 mm.
208
Jones & Dolan — Evolution of root hairs and rhizoids
water because of its tendency to bind to clay particles and form
insoluble precipitates in the soil (Brady and Weil, 2008). As a
result, there is little diffusion of phosphate through the soil
water to the root surface, where its concentration remains
low after uptake into the root. Consequently, the concentration
of phosphate of soil water in the vicinity of the root remains
low. This region surrounding the root where nutrients are
present in very low concentrations is known as a depletion
zone. The length of root hairs determines the size of this
zone. Plants with long root hairs develop large depletion
zones (the zone has a relatively large diameter), while plants
with short root hairs develop smaller depletion zones. Long
root hairs enable the plant to extract nutrients from a greater
volume of soil compared with plants with short root hairs (in
the absence of mycorrhizae) (Nye, 1966; Gahoonia and
Nielsen, 1996, 1998; Gahoonia et al., 1997). This explains
why root hair length is positively correlated with the ability
to absorb phosphate from the soil. Cultivars of barley with
short root hairs take up less phosphate than cultivars with
long root hairs when grown in field conditions with low available phosphate (Gahoonia and Nielsen, 1998, 2004).
Furthermore, root hairless barley mutants take up less phosphate from the soil and yield much less grain than wild-type
(long hair) cultivars in low phosphate conditions (Gahoonia
et al., 2001). The role of root hairs in the uptake of other nutrients with limited mobility in the soil has also been demonstrated. For example, the rate of K+ uptake from the soil is
also positively correlated with root hair length (Jungk,
2001). Together these data indicate that root hairs are important for the uptake of relatively immobile ions such as phosphate from the soil.
Mycorrhizae are symbioses between fungi and plants in
which fungi provide inorganic nutrients to the plant in exchange for reduced carbon compounds (Parniske, 2008).
Approximately 80 % of land plants develop symbioses with
glomeromycotan fungal partners called vesicular arbuscular
mycorrhizae (AM). Glomeromycota are obligate symbionts,
have been found in 411 million-year-old fossil plants from
the Rhynie Chert and are likely to have coevolved with the
land plants (Remy et al., 1994; Wang et al., 2010). They
form extensive hyphal networks in the soil and interface
with the plant at branched intracellular structures called arbuscules where nutrients and carbon compounds are exchanged.
There is a general trend among angiosperms that those
species that develop mycorrhizae tend to form relatively
short root hairs, while those that do not form mycorrhizae
develop relatively long root hairs (Baylis, 1975; St John,
1980). Given that the ability to form mycorrhizae is an ancestral state among land plants, and that many unrelated groups of
plants do not form mycorrhizae, it can be inferred that the
ability to form mycorrhizae was lost independently among different lineages of plants (such as the Brassicales) (reviewed in
Parniske, 2008). These non-mycorrhizal plants have evolved
long root hairs that facilitate nutrient uptake in the absence
of the fungal symbiont. Extreme examples of this are found
among the Cyperaceae, where some species that lack mycorrhizae growing in nutrient-poor soils develop ‘dauciform
roots’ where very long root hairs develop in patches along the
root system. The formation of cluster roots with very long
root hairs among species of the Proteaceae that lack
mycorrhizae is another example where long root hairs provide
the ability to extract limiting nutrients from the soil in the
absence of mycorrhizae (reviewed in Lambers et al., 2010).
RH IZO ID S HAVE ROLE S I N A NC HO RA GE A ND
T H E UP TA K E O F WAT E R A N D NU T R I E N T S
To date there have been few studies on the function of rhizoids, and what knowledge there is has been gleaned from
diverse species. Nevertheless there are indications that rhizoids
are important in anchorage and the uptake of water and nutrients. The examples presented here are from species that are
distantly related phylogenetically, and it should be borne in
mind that rhizoids may not carry out all of the above functions
in every species.
It is often asserted in the literature that the primary role of
rhizoids is in attachment to the substrate (Duckett et al.,
1998; Goffinet et al., 2008; Crandall-Stotler et al., 2009).
The rhizoids of many liverworts form discs or ramify at
their tips when they contact solid particles and adhere strongly
(Haberlandt, 1914; Odu and Richards, 1976; Pocock and
Duckett, 1985; Duckett et al., 1991). Similar branching has
also been observed at the tips of moss rhizoids in contact
with hard substrates (Duckett, 1994a; Pressel and Duckett,
2009), as well as in the rhizoids of filmy fern gametophytes
(Hymenophyllaceae) (Duckett et al., 1996), while moss rhizoids can also display thigmotropic responses, coiling around
objects in the substrate (Duckett, 1994b; Duckett and
Matcham, 1995). A role in attachment is also suggested by
the observation that, at least among the highly branched pleurocarpous mosses, rhizoids are more abundant and highly
branched in plants growing on bare, hard substrates such as
rocks than those growing on soil (Odu, 1978). Attachment to
the substrate may be facilitated by the production of adhesive
sulfated non-cellulose polysaccharides by rhizoid tips (Odu,
1989).
Rhizoids have also been shown to be involved in the uptake
and transport of water. Many bryophytes are ectohydric, i.e.
they lack thick cuticles and absorb water over their whole
surface (Proctor, 2000). Though rhizoids are not required for
direct uptake of water in these species, many mosses
produce a tomentum, a thick covering of rhizoids growing
from the stem, and the spaces that form between the hairs
aid water transport by capillary action (Proctor, 1984). In contrast, some bryophytes are endohydric, with internal water
transport. The rhizoids of the endohydric moss Polytrichum
have been shown to take up water from the substrate, though
the importance of this route of water uptake is probably
minor compared with uptake across aerial surfaces of the
plant (Mägdefrau, 1938; Trachtenberg and Zamski, 1979). In
the complex thalloid liverworts of the Marchantiales, rhizoids
are involved in the uptake and transport of water from the substrate. These liverworts possess two kinds of rhizoids: smoothwalled rhizoids and tuberculate rhizoids, the latter having pegshaped thickenings that project into the lumen of the rhizoid.
These thickened rhizoids form bundles (like the moss
tomenta) that run along the ventral surface of the thallus.
Aqueous dyes are rapidly transported by capillarity between
these rhizoids (Bowen, 1935; Czaja, 1936; McConaha, 1939,
1941; Kobiyama and Crandall-Stotler, 2011). In addition to
Jones & Dolan — Evolution of root hairs and rhizoids
this external movement along bundles of rhizoids, it has been
shown that water can travel inside both smooth-walled and tuberculate rhizoids, into the cells of the thallus surrounding the
rhizoid base (Kamerling, 1897; Clee, 1943). In Conocephalum
conicum and C. japonicum, the movement of water from the
rhizoids into the thallus is promoted by specialized pitted
cells on the ventral surface (Kobiyama and Crandall-Stotler,
2011). Together, these observations indicate that rhizoids are
important for water transport in the Marchantiales.
Rhizoids may be active in inorganic nutrient uptake in
diverse species. The rhizoids of Chara species grow into the
substrate where they play an important role in anchoring the
plant. In addition, these rhizoids contains a higher concentration of mineral nutrients than the open water (Barko et al.,
1991) and take up nitrate, ammonium and phosphates from
sediments (Box, 1986; Vermeer et al., 2003). There are, to
our knowledge, no reports demonstrating the role of liverwort
rhizoids in nutrient uptake. However, they often form
mycorrhiza-like associations with fungi (Read et al., 2000;
Russell and Bulman, 2005), which can substantially increase
the uptake of nutrients from the soil (Humphreys et al.,
2010). Nutrient acquisition by mosses is also not well understood, but it is generally thought that the majority of mosses
get most of their nutrients from precipitation and the deposition
of dust (Bates, 1992). Soil-growing mosses have been shown to
be able to obtain nutrients from the substrate (Chapin et al.,
1987; Bates and Farmer, 1990; Van Tooren et al., 1990),
though it has not been shown whether this is a result of direct
absorption by the rhizoids or external transport of nutrientbearing soil water over the plant surface to leafy parts.
Although the evidence is fragmentary, it seems that root
hairs and rhizoids carry out similar functions, albeit probably
to different extents in different species.
D O T H E S A M E G E N E S CO N T ROL T H E
DE VELO PMEN T OF ROOT H AI RS A ND
R HI Z OI DS ?
Much of our knowledge about the molecular and cellular
events during the development of root hairs comes from
studies in the model angiosperm Arabidopsis thaliana, where
the mechanisms of tip growth have been characterized in
some detail (reviewed, for instance, in Libault et al., 2010).
Less is known about the molecular and cellular events that
control the development of rhizoids.
Moss rhizoids develop on the gametophyte and, unlike root
hairs and the rhizoids of liverworts and hornworts, they are
multicellular. Root hairs and rhizoids probably have similar
functions as well as similar modes of growth and development.
However, it might be argued that they are analogous because
they are not structurally correspondent, since they are produced
by different phases of the life cycle (Scotland, 2010). It is possible that the resemblance between rhizoids and root hairs is a
result of convergent evolution because these cell types have
similar functions. Since the developmental mechanism for producing rhizoids already existed in early land plants, it is possible
that it was co-opted during the rise to dominance of the sporophyte, and deployed in a new context to produce root hairs. Do
rhizoids and root hairs share an ‘ancient toolkit’ of developmental genes?
209
There are preliminary indications that rhizoid and root hair
development may indeed share a common genetic mechanism.
Two related basic helix – loop – helix transcription factors,
ROOT HAIR DEFECTIVE 6 (AtRHD6) and ROOT HAIR
DEFECTIVE 6-LIKE 1 (AtRSL1), control root hair development in Arabidopsis. These proteins accumulate in cells that
will go on to develop root hairs, where they promote the transcription of genes necessary for tip growth such as ROOT
HAIR DEFECTIVE 6-LIKE 4 (RSL4) (Menand et al., 2007;
Yi et al., 2010). Mutants that lack AtRHD6 and AtRSL1 function do not develop root hairs (Menand et al., 2007; Yi et al.,
2010). Two similar genes were identified in the genome of the
model moss Physcomitrella patens and named PpRSL1 and
PpRSL2. Few rhizoids develop in double mutants that lack
both PpRSL1 and PpRSL2 function (Menand et al., 2007).
Furthermore, constitutive co-expression PpRSL1 and PpRSL2
transforms the gametophore into a mass of rhizoids (Jang
et al., 2011). These data indicate that PpRSL1 and PpRSL2 together are necessary and sufficient for rhizoid development.
This necessity and sufficiency indicate that these PpRSL
genes are key regulators of rhizoid development in mosses.
Remarkably, Arabidopsis mutants lacking RHD6 function
develop root hairs if transformed with the PpRSL1 gene
from Physcomitrella. This indicates that the function of RSL
proteins has been conserved for .420 million years since
mosses and vascular plants diverged from a common ancestor
(Menand et al., 2007). We propose that the RSL network was
co-opted to promote the formation of root hairs, when the freeliving vascular plant sporophyte increased in size and came
into contact with the soil. It is likely that at least some components of the regulatory network downstream of the RSL genes
have also been conserved during the intervening period, although this hypothesis remains to be tested.
Comparative genetic analyses have shown that changes in
the expression of regulatory genes have been important in
the evolution of morphological novelties in both animals and
plants, and that these changes often involve modifications to
the cis-regulatory regions of the genes (Carroll, 2008; De
Robertis, 2008; Shubin et al., 2009; Pires and Dolan, 2012;
Wittkopp and Kalay, 2012). Changes in the cis-regulatory
regions of RSL genes are likely to have played a role in altering
their expression during land plant evolution. RSL genes are
expressed in the gametophytes of non-vascular plants but not
in sporophytes. Changes in cis-regulatory elements could
have promoted the expression of RSL genes in the sporophyte
and repressed transcription in the gametophyte in vascular
plants. According to this model, expression of RSL genes in
sporophytes would then have initiated developmental programmes for rhizoid-like filamentous tip-growing cells (root
hairs) in this phase of the life cycle. Such changes in the cisregulatory regions of key genes may have played an important
role in the elaboration of the sporophyte as large multicellular
diploid plants rose to dominance during the Palaeozoic.
A U X I N PO S I T I V E LY RE G U L AT E S T H E
D E VELO PMEN T OF R HI ZOI DS A ND RO OT
H AI R S
Auxin signalling controls the rhizoid developmental programme that was probably redeployed in the sporophyte to
210
Jones & Dolan — Evolution of root hairs and rhizoids
control the development of root hairs. Auxin has a stimulatory
effect on rhizoid development in the alga Chara (Klämbt
et al., 1992), liverworts (Kaul et al., 1962; Maravolo and Voth,
1966) and ferns (Hickok and Kiriluk, 1984). Physcomitrella
mutants defective in auxin perception develop few rhizoids; conversely, the application of auxin to wild-type plants promotes the
development of supernumerary rhizoids (Ashton et al., 1979;
Sakakibara et al., 2003; Prigge et al., 2010). Auxin controls
the development of Physcomitrella rhizoids by regulating the expression of PpRSL1 and PpRSL2 genes (Jang et al., 2011). This
indicates that RSL genes and auxin signalling interact during the
development of rhizoids.
Auxin positively regulates root hair development in angiosperms. In Arabidopsis, auxin gradients generated by auxin
influx carriers are responsible for limiting the position of
root hair initiation to the region of the cell closest to the root
tip, since root hairs develop in more shootward parts of the
cell in mutants with defective auxin signalling (Pitts et al.,
1998; Grebe et al., 2002; Ikeda et al., 2009). Furthermore,
auxin positively regulates root hair elongation; the root hairs
of auxin signalling mutants are shorter than in the wild type
(Pitts et al., 1998; Knox et al., 2003). Auxin exerts this
effect at least partly by influencing the expression of the
gene encoding the RSL4 basic helix – loop – helix transcription
factor (Yi et al., 2010). Treatment with auxin increases the
transcription of RSL4, which is required for root hair growth;
these data indicate that auxin stimulates root hair elongation
by increasing the transcription of RSL4. In Physcomitrella,
auxin promotes the expression of different genes – PpRSL1
and PpRSL2 and not orthologs of RSL4 (Jang and Dolan,
2011). Despite this difference, these data suggest that auxin
and RSL genes are part of an ancient genetic network controlling the development of rooting cells that was present in the
last common ancestor of mosses and vascular plants (Jang
and Dolan, 2011).
CO NCL USI ON S
Character mapping on current phylogenies implies that the
earliest land plant life cycles resembled that of extant liverworts in which the gametophyte was free living and the sporophyte was embedded in the gametophyte. If true, this suggests
that the regulatory module controlling rhizoid and root hair development first operated in the gametophyte of early land
plants. We propose that this regulatory module became
expressed in sporophytes as the diploid phase became free
living, developing filamentous cells at the interface of the
plant and soil. If such transference of regulatory modules
between phases of the plant life cycle is widespread, it
could, at least in part, explain the genetic basis for the increase
in the morphological diversity of sporophytes that occurred
during the radiation of land plants in the Devonian Period.
OU TLO OK AN D OU TSTA ND IN G Q UES T IO NS
An ancient mechanism controls the development of filamentous
cells at the plant–soil interface in mosses and angiosperms.
How ancient is this mechanism? Was the development of filamentous rooting cells at the plant–soil interface an evolutionary
novelty acquired by the ancestor of all land plants during the
conquest of the land? Or was the mechanism already present in plants’ algal ancestors, a pre-existing developmental
network that facilitated the transition to the terrestrial environment? Characterization of the genetic networks controlling the
development of rhizoids in liverworts and streptophyte algae
will allow us to answer this question.
Often a trait that has evolved multiple times in independent
lineages is the result of wiring the same ancestral genes in new
ways, as seen, for example, in the reduction of pelvic structures
in separate stickleback populations (Shapiro et al., 2004; Chan
et al., 2010), the convergent evolution of butterfly wing patterns (Reed et al., 2011) and the independent evolution of
wing spots in different Drosophila species (Gompel et al.,
2005; Prud’homme et al., 2006). Roots bearing root hairs
probably evolved independently on at least two separate occasions (among the lycophytes and euphyllophytes). Was the
same network co-opted on each occasion to regulate the development of root hairs? This question can be addressed by characterizing the genetic control of root hair growth and the roles
of RSL genes in the lycophyte Selaginella moellendorffii, the
genome sequence of which has recently been published
(Banks et al., 2011).
The possible role of changes in cis-regulatory elements in
the co-option of genes controlling rhizoid development has
not been examined. cis-regulatory elements specific to root
hairs have been identified in angiosperms (Cho and
Cosgrove, 2002; Kim et al., 2006; Won et al., 2009). The characterization of further rhizoid-specific genes and their regulatory elements in basally diverging plants will allow us to
assess the importance of changes in cis-regulatory elements
in re-wiring a rhizoid developmental programme to give root
hairs on the sporophyte.
ACK N OW L E DG E M E N T S
We thank John Baker for photographic assistance; Clemence
Bonnot, Andrew Plackett, Heather Sanders, Thomas Tam and
Eftychios Frangedakis for plant material; and James Doyle for
helpful comments on the manuscript. This work is supported
by a Newton-Abraham Studentship at the University of Oxford
to V.A.S.J., and grants from the European Union–Marie
Curie–Integrated Training Network (PLANTORIGINS),
European Research Council (EVO500) and the Biotechnology
and Biological Science Research Council of the UK to L.D.
L I T E R AT U R E C I T E D
Ashton NW, Grimsley NH, Cove DJ. 1979. Analysis of gametophytic development in the moss, Physcomitrella patens, using auxin and cytokinin resistant mutants. Planta 144: 427– 435.
Banks JA. 1999. Gametophyte development in ferns. Annual Review of Plant
Physiology and Plant Molecular Biology 50: 163– 186.
Banks JA. 2009. Selaginella and 400 million years of separation. Annual
Review of Plant Biology 60: 223– 238.
Banks JA, Nishiyama T, Hasebe M, et al. 2011. The Selaginella genome
identifies genetic changes associated with the evolution of vascular
plants. Science 332: 960– 963.
Barko JW, Gunnison D, Carpenter SR. 1991. Sediment interactions with
submersed macrophyte growth and community dynamics. Aquatic
Botany 41: 41– 65.
Bateman RM, Crane PR, Dimichele WA, et al. 1998. Early evolution of land
plants: phylogeny, physiology, and ecology of the primary terrestrial
Jones & Dolan — Evolution of root hairs and rhizoids
radiation. Annual Review of Ecology, Evolution, and Systematics 29:
263– 292.
Bates JW. 1992. Mineral nutrient acquisition and retention by bryophytes.
Journal of Bryology 17: 223–240.
Bates JW, Farmer AM. 1990. An experimental study of calcium acquisition
and its effects on the calcifuge moss Pleurozium schreberi. Annals of
Botany 65: 87– 96.
Baylis GTS. 1975. The magnoloid mycorrhiza and mycotrophy in root
systems derived from it. In: Sanders FE, Mosse B, Tinker PB. eds.
Endomycorrhizae. New York: Academic Press, 373– 389.
Berner RA. 1997. The rise of plants and their effect on weathering and atmospheric CO2. Science 276: 544– 546.
Bowen EJ. 1935. A note on the conduction of water in Fimbriaria bleumeana.
Annals of Botany 49: 844–848.
Box RJ. 1986. Quantitative short-term uptake of inorganic phosphate by the
Chara hispida rhizoid. Plant, Cell and Environment 9: 501– 506.
Brady NC, Weil RR. 2008. The nature and properties of soils. Upper Saddle
River, NJ: Pearson-Prentice Hall.
Carol RJ, Dolan L. 2002. Building a hair: tip growth in Arabidopsis thaliana
root hairs. Philosophical Transactions of the Royal Society B: Biological
Sciences 375: 815– 821.
Carroll SB. 2008. Evo-devo and an expanding evolutionary synthesis: a
genetic theory of morphological evolution. Cell 134: 25– 36.
Chan YF, Marks ME, Jones FC, et al 2010. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science
327: 302–305.
Chapin FSI, Oechel WS, Van Cleve K, Lawrence W. 1987. The role of
mosses in the phosphorous cycling of an Alaskan black spruce forest.
Oecologia 74: 310– 315.
Cho H-T, Cosgrove DJ. 2002. Regulation of root hair initiation and expansin
gene expression in Arabidopsis. The Plant Cell 14: 3237– 3253.
Clee DA. 1943. The morphology and anatomy of Fegatella conica in relation
to the mechanism of absorption and conduction of water. Annals of
Botany VII: 185 –193.
Crandall-Stotler B, Stotler RE. 2008. Morphology and classification of the
Marchantiophyta. In: Shaw A, Goffinet B. eds. Bryophyte biology.
New York: Cambridge University Press, 1 –54.
Czaja AT. 1936. Untersuchungen über den Membraneffekt des
Absorptionsgewebes und über die Farbstoffaufnahme in die lebende
Zelle. Planta 26: 90–119.
De Robertis EM. 2008. Evo-devo: variations on ancestral themes. Cell 132:
185– 195.
Dittmer HJ. 1949. Root hair variations in plant species. American Journal of
Botany 36: 152–155.
Duckett JG. 1994a. Studies of protonemal morphogenesis in mosses VI. The
foliar rhizoids of Calliergon stramineum (Brid.) Kindb. function as
organs of attachment. Journal of Bryology 18: 239–252.
Duckett JG. 1994b. Studies of protonemal morphogenesis in mosses. V.
Diphyscium foliosum (Hedw.) Mohr. (Buxbaumiales). Journal of
Bryology 18: 223–238.
Duckett JG, Matcham HW. 1995. Studies of protonemal morphogenesis in
mosses. VIII. The perennial rhizoids and gemmiferous protonema of
Dicranella heteromalla (Hedw.) Schimp. Journal of Bryology 18: 407–
424.
Duckett JG, Renzaglia KS, Pell K. 1991. A light and electron microscope
study of rhizoid–ascomycete associations and flagelliform axes in
British hepatics with observations on the effects of the fungi on host
morphology. New Phytologist 118: 233–257.
Duckett JG, Russell AJ, Ligrone R. 1996. Trichomes in the
Hymenophyllaceae. In: Camus JM, Gibby M, Johns RJ. eds.
Pteridology in perspective. Kew: Royal Botanic Gardens, 511– 514.
Duckett JG, Schmid AM, Ligrone R. 1998. Protonemal morphogenesis. In:
Bates JW, Ashton NW, Duckett JG. eds. Bryology for the twenty-first
century. Leeds, UK: British Bryological Society, 223 –246.
Finet C, Timme RE, Delwiche CF, Marlétaz F. 2010. Multigene phylogeny
of the green lineage reveals the origin and diversification of land plants.
Current Biology 20: 2217– 2222.
Föhse D, Claassen N, Jungk A. 1991. Phosphorus efficiency of plants II.
Significance of root radius, root hairs and cation–anion balance for phosphorus influx in seven plant species. Plant and Soil 132: 261– 272.
Friedman WE, Moore RC, Purugganan MD. 2004. The evolution of plant
development. American Journal of Botany 91: 1726– 1741.
211
Gahoonia TS, Nielsen NE. 1996. Variation in acquisition of soil phosphorus
among wheat and barley genotypes. Plant and Soil 178: 223– 230.
Gahoonia TS, Nielsen NE. 1997. Variation in root hairs of barley cultivars
doubled soil phosphorus uptake. Euphytica 98: 177–182.
Gahoonia TS, Nielsen NE. 1998. Direct evidence on participation of root
hairs in phosphorus (32P) uptake from soil. 198: 147– 152.
Gahoonia TS, Nielsen NE. 2004. Barley genotypes with long root hairs
sustain high grain yields in low-P field. Plant and Soil 262: 55–62.
Gahoonia TS, Care D, Nielsen NE. 1997. Root hairs and phosphorus acquisition of wheat and barley cultivars. Plant and Soil 191: 181– 188.
Gahoonia TS, Nielsen NE, Joshi PA, Jahoor A. 2001. A root hairless barley
mutant for elucidating genetics of root hairs and phosphorus uptake. Plant
and Soil 235: 211– 219.
Gensel PG, Berry CM. 2001. Early lycophyte evolution. American Fern
Journal 91: 74– 98.
Gensel PG, Kotyk M, Basinger J. 2001. Morphology of above- and belowground structures in early Devonian (Pragian-Emsian) plants. In:
Gensel PG. ed. Plants invade the land: evolutionary and environmental
perspectives. New York: Columbia University Press, 83– 102.
Goffinet B, Buck WR, Shaw AJ. 2008. Morphology, anatomy and classification of the Bryophyta. In: Shaw A, Goffinet B. eds. Bryophyte biology.
New York: Cambridge University Press, 55–138.
Gompel N, Prud’homme B, Wittkopp PJ, Kassner VA, Carroll SB. 2005.
Chance caught on the wing: cis-regulatory evolution and the origin of
pigment patterns in Drosophila. Nature 433: 481 –487.
Grebe M, Friml J, Swarup R, et al 2002. Cell polarity signaling in
Arabidopsis involves a BFA-sensitive auxin influx pathway. Current
Biology 12: 329–334.
Haberlandt GFJ. 1914. Physiological plant anatomy [Translated from the 4th
German ed. by M. Drummond]. London: MacMillan & Co.
Hickok LG, Kiriluk RM. 1984. Effects of auxins on gametophyte development and sexual differentiation in the fern Ceratopteris thalictroides
(L.) Brongn. Botanical Gazette 145: 37– 42.
Hofmeister W. 1851. Vergleichende Untersuchungen der Keimung,
Entfaltung und Fruchtbildung höherer Kryptogamen (Moose, Farrn,
Equisetaceen, Rhizocarpeen und Lycopodiaceen) und der Samenbildung
der Coniferen. Leipzig: Verlag F. Hofmeister.
Humphreys CP, Franks PJ, Rees M, Bidartondo MI, Leake JR, Beerling
DJ. 2010. Mutualistic mycorrhiza-like symbiosis in the most ancient
group of land plants. Nature Communications 1: 103.
Ikeda Y, Men S, Fischer U, Stepanova AN, Alonso JM, Ljung K, Grebe M.
2009. Local auxin biosynthesis modulates gradient-directed planar polarity in Arabidopsis. Nature Cell Biology 11: 731–738.
Jang G, Dolan L. 2011. Auxin promotes the transition from chloronema to
caulonema in moss protonema by positively regulating PpRSL1and
PpRSL2 in Physcomitrella patens. New Phytologist 192: 319 –327.
Jang G, Yi K, Pires ND, Menand B, Dolan L. 2011. RSL genes are sufficient
for rhizoid system development in early diverging land plants.
Development 138: 2273– 2281.
Jungk A. 2001. Root hairs and the acquisition of plant nutrients from soil.
Journal of Plant Nutrition and Soil Science 164: 121– 129.
Kamerling Z. 1897. Zur Biologie und Physiologie der Marchantiaceen. Flora
84: 1 –68.
Karol KG, McCourt RM, Cimino MT, Delwiche CF. 2001. The closest
living relatives of land plants. Science 294: 2351–2353.
Kaul K, Mitra G, Tripathi B. 1962. Responses of Marchantia in aseptic
culture to well-known auxins and antiauxins. Annals of Botany 26: 447.
Kenrick PR, Crane PR. 1997a. The origin and early evolution of plants on
land. Nature 389: 33– 39.
Kenrick PR, Crane PR. 1997b. The origin and early diversification of land
plants: a cladistic study. Washington, DC: Smithsonian Institution Press.
Kidston R, Lang WH. 1920. On Old Red Sandstone plants showing structure,
from the Rhynie Chert bed, Aberdeenshire. Part III Asteroxylon mackiei,
Kidston and Lang. Transactions of the Royal Society of Edinburgh 52:
643–688.
Kim DW, Lee SH, Choi S-B, et al 2006. Functional conservation of a root
hair cell-specific cis-element in angiosperms with different root hair distribution patterns. The Plant Cell 18: 2958–70.
Klämbt D, Knauth B, Dittmann I. 1992. Auxin dependent growth of rhizoids
of Chara globularis. Physiologia Plantarum 85: 537–540.
Knox K, Grierson CS, Leyser O. 2003. AXR3 and SHY2 interact to regulate
root hair development. Development 130: 5769– 5777.
212
Jones & Dolan — Evolution of root hairs and rhizoids
Kobiyama Y, Crandall-Stotler B. 2011. Studies of specialized pitted parenchyma cells of the liverwort Conocephalum Hill and their phylogenetic
implications. International Journal of Plant Sciences 160: 351–370.
Lambers H, Brundrett MC, Raven JA, Hopper S. 2010. Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils
is linked to functional diversity for nutritional strategies. Plant and Soil
334: 11–31.
Leliaert F, Smith DR, Moreau H, et al 2012. Phylogeny and molecular evolution of the green algae. Critical Reviews in Plant Sciences 31: 1– 46.
Lenton TM, Crouch M, Johnson M, Pires N, Dolan L. 2012. First plants
cooled the Ordovician. Nature Geoscience 5: 86–89.
Lewis LA, McCourt RM. 2004. Green algae and the origin of land plants.
American Journal of Botany 91: 1535– 1556.
Libault M, Brechenmacher L, Cheng J, Xu D, Stacey G. 2010. Root hair
systems biology. Trends in Plant Science 15: 641– 650.
Maravolo NC, Voth PD. 1966. Morphogenic effects of three growth substances on Marchantia gemmalings. Botanical Gazette 127: 79– 86.
Marschner P. 2012. Marschner’s mineral nutrition of higher plants. London:
Academic Press.
Mägdefrau K. 1938. Reviews of recent research 2. Der Wasserhaushalt der
Moose. Annales Bryologici 10: 141– 150.
McConaha M. 1939. Ventral surface specializations of Conocephalum
conicum. American Journal of Botany 26: 353–355.
McConaha M. 1941. Ventral structures effecting capillarity in the
Marchantiales. American Journal of Botany 28: 301– 306.
McManus HA, Qiu Y-L. 2008. Life cycles in major lineages of photosynthetic eukaryotes, with a special reference to the origin of land plants.
Fieldiana Botany 47: 17– 33.
Menand B, Yi K, Jouannic S, et al 2007. An ancient mechanism controls the
development of cells with a rooting function in land plants. Science 316:
1477–1480.
Nye PH. 1966. The effect of the nutrient intensity and buffering power of a
soil, and the absorbing power, size and root hairs of a root, on nutrient
absorption by diffusion. Plant and Soil 25: 81–105.
Odu EA. 1978. The adaptive importance of moss rhizoids for attachment to
the substratum. Journal of Bryology 10: 163–181.
Odu EA. 1989. Extracellular adhesive substances on bryophyte rhizoids. Acta
Botanica Hungarica 35: 273– 277.
Odu EA, Richards P. 1976. The stimulus to branching of the rhizoid tip in
Lophocolea cuspidata (Nees) Limpr. Journal of Bryology 9: 93–105.
Parniske M. 2008. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nature Reviews Microbiology 6: 763–775.
Pearson HM. 1969. Rhizoids and root hairs of ferns. American Fern Journal
59: 107–122.
Pires ND, Dolan L. 2012. Morphological evolution in land plants: new
designs with old genes. Philosophical Transactions of the Royal Society
B: Biological Sciences 367: 508– 518.
Pitts RJ, Cernac A, Estelle M. 1998. Auxin and ethylene promote root hair
elongation in Arabidopsis. The Plant Journal 16: 553–560.
Pocock K, Duckett JG. 1985. On the occurence of branched and swollen rhizoids in British hepatics: their relationships with the substratum and associations with fungi. New Phytologist 99: 281–304.
Pressel S, Duckett JG. 2009. Studies of protonemal morphogenesis in mosses.
XII. Ephemeropsis, the zenith of morphological differentiation. Journal
of Bryology 31: 67–75.
Pressel S, Ligrone R, Duckett JG. 2008. Cellular differentiation in moss protonemata: a morphological and experimental study. Annals of Botany
102: 227– 245.
Prigge MJ, Lavy M, Ashton NW, Estelle M. 2010. Physcomitrella patens
auxin-resistant mutants affect conserved elements of an auxin-signaling
pathway. Current Biology 20: 1907–1912.
Proctor MCF. 1984. Structure and ecological adaptation. In: Dyer AF,
Duckett JG. eds. The experimental biology of bryophytes. London:
Academic Press, 9– 37.
Proctor MCF. 2000. The bryophyte paradox: tolerance of desiccation, evasion
of drought. Plant Ecology 151: 41–49.
Prud’homme B, Gompel N, Rokas A, et al. 2006. Repeated morphological
evolution through cis-regulatory changes in a pleiotropic gene. Nature
440: 1050–1053.
Qiu Y-L, Li L, Wang B, et al. 2006. The deepest divergences in land plants
inferred from phylogenomic evidence. Proceedings of the National
Academy of Sciences, USA 103: 15511–15516.
Qiu Y-L, Li L, Wang B, et al 2007. A nonflowering land plant phylogeny inferred from nucleotide sequences of seven chloroplast, mitochondrial, and
nuclear genes. International Journal of Plant Sciences 168: 691– 708.
Raven JA, Edwards D. 2001. Roots: evolutionary origins and biogeochemical
significance. Journal of Experimental Botany 52: 381– 401.
Read DJ, Duckett JG, Francis R, Ligrone R, Russell A. 2000. Symbiotic
fungal associations in ‘lower’ land plants. Philosophical Transactions
of the Royal Society B: Biological Sciences 355: 815– 830; discussion
830– 831.
Reed RD, Papa R, Martin A, et al 2011. optix drives the repeated convergent
evolution of butterfly wing pattern mimicry. Science 333: 1137–1141.
Remy W, Taylor TN, Hass H, Kerp H. 1994. Four hundred-million-year-old
vesicular arbuscular mycorrhizae. Proceedings of the National Academy
of Sciences, USA 91: 11841–11843.
Renzaglia KS, Villarreal JC, Duff RJ. 2008. New insights into morphology,
anatomy, and systematics of hornworts. In: Shaw A, Goffinet B. eds.
Bryophyte biology. New York: Cambridge University Press, 139– 171.
Rubinstein CV, Gerrienne P, de la Puente GS, Astini RA, Steemans P.
2010. Early Middle Ordovician evidence for land plants in Argentina
(eastern Gondwana). New Phytologist 188: 365–369.
Russell J, Bulman S. 2005. The liverwort Marchantia foliacea forms a specialized symbiosis with arbuscular mycorrhizal fungi in the genus Glomus.
New Phytologist 165: 567–579.
Sakakibara K, Nishiyama T, Sumikawa N, Kofuji R, Murata T, Hasebe M.
2003. Involvement of auxin and a homeodomain-leucine zipper I gene in
rhizoid development of the moss Physcomitrella patens. Development
130: 4835– 46.
Schneider H, Pryer KM, Cranfill R, Smith AR, Wolf PG. 2002. Evolution
of vascular plant body plans: a phylogenetic perspective. In: Cronk QCB,
Bateman RM, Hawkins JA. eds. Developmental genetics and plant evolution. London: Taylor & Francis, 330–364.
Scotland RW. 2010. Deep homology: a view from systematics. BioEssays 32:
438– 449.
Shapiro MD, Marks ME, Peichel CL, et al. 2004. Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks.
Nature 428: 717– 723.
Shubin N, Tabin C, Carroll S. 2009. Deep homology and the origins of evolutionary novelty. Nature 457: 818– 823.
St John TV. 1980. Root size, root hairs and mycorrhizal infection: a reexamination of Baylis’s hypothesis with tropical trees. New Phytologist 84: 483 –
487.
Strasburger E. 1894. Uber periodische Reduction der Chromosomenzahl im.
Entwicklungsgang der Organismen. Biologisches Centralblatt 14: 817 –
838; 849–866.
Trachtenberg S, Zamski E. 1979. The apoplastic conduction of water in
Polytrichum juniperinum Willd. gametophytes. New Phytologist 83:
49–52.
Van Tooren BF, Van Dam D, During HJ. 1990. The relative importance of
precipitation and soil as sources of nutrients for Calliergonella cuspidata
(Hedw.) Loeske in chalk grassland. Functional Ecology 4: 101–107.
Vermeer C, Escher M, Portielje R, de Klein JJM. 2003. Nitrogen uptake
and translocation by Chara. Aquatic Botany 76: 245–258.
Wang B, Yeun LH, Xue J-Y, Liu Y, Ané J-M, Qiu Y-L. 2010. Presence of
three mycorrhizal genes in the common ancestor of land plants suggests a
key role of mycorrhizas in the colonization of land by plants. New
Phytologist 186: 514– 525.
Wellman CH, Osterloff PL, Mohiuddin U. 2003. Fragments of the earliest
land plants. Nature 425: 282–285.
Wittkopp PJ, Kalay G. 2012. Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nature Reviews
Genetics 13: 59– 69.
Wodniok S, Brinkmann H, Glöckner G, et al. 2011. Origin of land plants:
do conjugating green algae hold the key? BMC Evolutionary Biology
11: 104.
Won S-K, Lee Y-J, Lee H-Y, Heo Y-K, Cho M, Cho H-T. 2009.
Cis-element- and transcriptome-based screening of root hair-specific
genes and their functional characterization in Arabidopsis. Plant
Physiology 150: 1459–1473.
Yi K, Menand B, Bell E, Dolan L. 2010. A basic helix–loop– helix transcription factor controls cell growth and size in root hairs. Nature Genetics 42:
264– 267.