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J
IPB Journal of Integrative
Plant Biology Invited Expert Review
https://doi.org/10.1111/jipb.13224
Origin and evolution of green plants in the light of key
evolutionary events
FA
Zhenhua Zhang , Xiaoya Ma , Yannan Liu , Lingxiao Yang , Xuan Shi , Hao Wang , Runjie Diao and
Bojian Zhong*
College of Life Sciences, Nanjing Normal University, Nanjing 210023, China
*Correspondence: Bojian Zhong (bjzhong@gmail.com)
Zhenhua Zhang Bojian Zhong
ABSTRACT
Green plants (Viridiplantae) are ancient photo-
synthetic organisms that thrive both in aquatic
and terrestrial ecosystems, greatly contributing
to the changes in global climates and ecosys-
tems. Significant progress has been made to-
ward understanding the origin and evolution of
green plants, and plant biologists have arrived
at the consensus that green plants first
originated in marine deep‐water environments
and later colonized fresh water and dry land.
The origin of green plants, colonization of land
by plants and rapid radiation of angiosperms
arethreekeyevolutionaryeventsduringthe
long history of green plants. However, the
comprehensive understanding of evolutionary
features and molecular innovations that en-
abled green plants to adapt to complex and
changeable environments are still limited. Here,
we review current knowledge of phylogenetic
relationships and divergence times of green
plants, and discuss key morphological in-
novations and distinct drivers in the evolution
of green plants. Ultimately, we highlight funda-
mental questions to advance our understanding
of the phenotypic novelty, environmental
adaptation, and domestication of green plants.
Keywords: adaptation, divergence times, green plants, key
innovations, phylogenetics, terrestrialization
Zhang, Z., Ma, X., Liu, Y., Yang, L., Shi, X., Wang, H., Diao, R.,
and Zhong, B. (2022). Origin and evolution of green plants in the
light of key evolutionary events. J. Integr. Plant Biol. 64: 516–535.
INTRODUCTION
The primary endosymbiotic event gave rise to three pho-
tosynthetic lineages, including green plants (Vir-
idiplantae), red algae (Rhodophyta) and Glaucophyta, which
together formed the Archaeplastida. Over millions of years of
evolution, multiple lineages of the ancient photosynthetic
eukaryotes have successfully adapted to terrestrial environ-
ments (Raven and Edwards, 2014). Among these organisms,
green plants are the most successful group, and show
high biodiversity and wide distribution in subaerial/terrestrial
habitats, comprising ~450,000−500,000 species (Guiry,
2012;Corlett, 2016). Green plants originated from the primary
endosymbiotic event, which probably took place in the Pa-
laeoproterozoic, around 1.2 billion years ago, the engulfment
of a cyanobacterium by a heterotrophic unicellular
eukaryote (Dagan et al., 2013;de Vries et al., 2016;Leliaert
et al., 2019).
Green plants are the major groups of oxygenic photo-
synthetic eukaryotes, including green algae and their de-
scendants: streptophyte algae (charophytes) and land plants
(embryophytes) (Leliaert et al., 2012). Green algae include
two major groups: Chlorophyta, the well‐documented ancient
photosynthetic eukaryotes; and Prasinodermophyta, a novel
phylum that diverged before the split of Chlorophyta and
Streptophyta (Figure 1;Leliaert et al., 2016;Li et al., 2020).
Green algae are not only of particularly evolutionary interest
due to their high morphological and cytological diversity, but
also their great contribution to the global ecosystem
(Charlson et al., 1987;Gage et al., 1997;De Clerck et al.,
2018). The origin and diversification of green algae lays the
foundations for the modern diversity of green plants, and this
© 2022 Institute of Botany, Chinese Academy of Sciences
key evolutionary event is often regarded as the starting point
in the evolution of green plants.
The origin and evolution of streptophyte algae (char-
ophytes) and land plants from a green algal ancestor is the
second key evolutionary event in the history of green plants
(Figure 2). The colonization of the terrestrial realms by early
land plants remarkably contributes to the increase of primary
productivity and new habitats for animals that increased their
diversity (Parnell and Foster, 2012;One Thousand Plant
Transcriptomes Initiative, 2019). Which specific lineage of
streptophyte algae gave rise to land plants is the fundamental
question in tracing the evolutionary history of land plants.
Recent large‐scale phylogenomic studies based on plastid
and nuclear genes supported that the Zygnematophyceae
was the sister group to land plants, which had simple cyto‐
morphology (i.e., unicellular and filamentous) (Zhong et al.,
2013,2014;One Thousand Plant Transcriptomes Initiative,
2019). Interestingly, in higher‐branching streptophyte algae
(the Zygnematophyceae, Coleochaetophyceae and Char-
ophyceae grade, the ZCC grade), Zygnematophyceae are
simple unicellular and filamentous forms, and Chara from
Charophyceae possess high degrees of organismal com-
plexity, such as the stonewort with rhizoids and stem‐like
structures (Hori et al., 2014;Nishiyama et al., 2018;Cheng
et al., 2019;Liang et al., 2020). Thus, the origin of land plants
is referred to as the evolutionary singularity, due to the
enigmatic origin of various traits of land plants.
The flourishing of seed plants has shaped the terrestrial
ecosystem, and angiosperms undoubtedly dominated recent
ecological history on land. Angiosperms have surpassed
gymnosperms to be the most diverse land plants, due to a
rapid radiation and diversification around 130 Ma (Figure 2).
The rapid radiation and diversification of angiosperms is the
third key evolutionary event, which has been referred to as
the Darwin's “abominable mystery”(Friedman, 2009;
Augusto et al., 2014). Approximately 99.95% of the angio-
sperms form a clade called Mesangiospermae, including five
major groups: eudicots, monocots, magnoliids, Chlor-
anthales, and Ceratophyllales. The phylogenetic relationships
among these five groups have been the subject of long de-
bate (Zeng et al., 2014;One Thousand Plant Transcriptomes
Initiative, 2019;Yang et al., 2020a;Guo et al., 2021;Ma et al.,
2021). The increasing genomic data largely increased the
resolution of phylogenetic relationships of Mesangio-
spermae, and an accurate phylogeny would provide oppor-
tunities to elucidate the mechanisms underpinning their ra-
diation and understanding of evolution of innovative traits.
Here, we review recent progresses in the elucidation of
origin and evolutionary scenarios of green plants, mainly fo-
cusing on the three key evolutionary events. We discuss the
phylogenetic affinities of green plants, propose a reliable
timescale for plant evolution, and summarize the adaptive
mechanisms of green plants that enabled their adaptations
and diversifications. This review expands our knowledge of
the evolution of green plants and highlights key scientificis-
sues that require further investigations in plant evolution.
THE PHYLOGENETIC
RELATIONSHIP AND TIMESCALE
OF EARLY GREEN PLANTS
Complex phylogenetic affinities of green algae
Early green plants initially diversified as unicellular plank-
tonic algae in the oceans, and gave rise to the Prasino-
dermophyta and Chlorophyta. Unicellular green algae from
early diverging lineages were referred to as prasinophytes,
and approximately nine clades of the prasinophytes were
identified, forming a paraphyletic assemblage of scaled/
naked, flagellated/non‐flagellated microalgae (Leliaert et al.,
2012;Lemieux et al., 2014;Fang et al., 2017;Leliaert et al.,
2019). Recent phylogenomic studies have greatly improved
the relationships of prasinophytes. The Prasinococcales
(clade VI) together with the Palmophyllales (Palmophyllo-
phyceae) occupied the deepest branch of the prasinophytes
(Leliaert et al., 2016). The Pyramimonadales (clade I)+Ma-
miellophyceae (clade II) formed the second‐deepest clade,
and the more recently diverging groups included the
Nephroselmidophyceae (clade III), Pycnococcaceae (clade
V) and other lineages (clades VIIA and VIIC) (Lopes dos
Santos et al., 2017). Notably, the circumscription of the
prasinophytes has changed with the Prasinoderma coloniale
genome, which placed Palmophyllophyceae as the earliest‐
branching green plants, unveiling the existence of a novel
phylum within green plants–the Prasinodermophyta (Figure 1;
Li et al., 2020). This finding underscores the need for generating
more genomic resources for early branching green algae, which
will shed new light on the evolutionary routes of early green
plants.
Figure 1. The phylogeny, ecology and morphology of green algae
The phylogeny of the main lineages of green algae is a composite of widely
accepted relationships based on molecular data (Leliaert et al., 2019;Del
Cortona et al., 2020;Li et al., 2020,2021a). Uncertain phylogenetic rela-
tionships are indicated by polytomies. Different colors indicate the main
habitats of each lineage: blue‐marine; green‐freshwater; orange‐terrestrial.
The drawings show the main morphology of each lineage, and illustrate the
transformation from ancestral unicellularity to complex multicellularity in
green algae. Ulvophyceae s.s. represents the Ulvophyceae lineage except
for Bryopsidales.
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Prasinophytes gave rise to the core Chlorophyta that in-
cludes unicellular and multicellular species, a major group of
green algae diversified in marine, freshwater and terrestrial
environments. The core Chlorophyta includes three large
classes (Ulvophyceae, Trebouxiophyceae and Chlor-
ophyceae: UTC) and two small classes (Pedinophyceae and
Chlorodendrophyceae) (Figure 1). The monophyletic group of
Chlorophyceae have been widely supported by both molec-
ular and ultrastructural data (Mattox and Stewart, 1984;
Lemieux et al., 2015;Fučíková et al., 2016;Sun et al.,
2016;Fang et al., 2018). In terms of Trebouxiophyceae, re-
cent nuclear phylogenomic analyses yielded phylogenetic
trees that were congruent with that from chloroplast ge-
nomes (Del Cortona et al., 2020;Li et al., 2021a). These tree
topologies highly supported that Trebouxiophyceae, the
earliest diverging branch of UTC, was a monophyletic group,
comprising two different branches: Chlorellales and core
Trebouxiophyceae. Ulvophyceae has been resolved as pol-
yphyletic, including two monophyletic groups: Bryopsidales
and remaining Ulvophyceae (hereafter Ulvophyceae s.s.)
(Fang et al., 2018;Del Cortona et al., 2020;Li et al., 2021a).
Pedinophyceae and Chlorodendrophyceae were the early‐
diverging groups of the core Chlorophyta, while their
branching order remained in conflict (Fang et al., 2018;Li
et al., 2021a).
Reconstructing an accurate phylogeny of anciently di-
verged lineages of green plants presents a serious challenge,
mainly due to the poor taxon sampling, molecular rate
Figure 2. The evolutionary relationship, fossils and morphological evolution of green plants
The tree topology is a composite of widely accepted relationships based on phylogenomic evidences (One Thousand Plant Transcriptomes Initiative,
2019;Guo et al., 2021;Ma et al., 2021). Dotted line indicates the controversial relationships in current studies. Different life cycles and presence/absence of
stomata in various lineages of green plants are shown. The red circles represent the ages of the oldest known fossils of green plants, embryophytes and
angiosperms. The fossil images are derived from Qing Tang, Strother and Foster (2021) and Hughes and McDougall (1990).
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heterogeneity, and limitation of phylogenetic resolution pro-
vided by current phylogenetic methods (Leliaert et al.,
2011,2016). The phylogenetic incongruence among the five
major classes within the core Chlorophyta are subject to the
rate variation across lineages and amino acid/nucleotide
compositional variation (Liu et al., 2014). The homogeneous
models could not fully consider the rate variation and com-
positional heterogeneity and instead exacerbate model mis-
specification issues, which considerably reduce the phylo-
genetic accuracy of green algae (Kapli et al., 2020). Fang
et al. (2018) found that the main conflicts in chloroplast
phylogeny of core Chlorophyta likely stem from the sub-
stantial GC‐heterogeneous sites. The phylogenetic inference
of core Chlorophyta was greatly improved by progressively
removing the most GC‐heterogeneous sites and applying
heterogeneous models. Moreover, it is worth noting that
large‐scale datasets dramatically reduced stochastic errors
in phylogenetic inference, but they simultaneously amplified
systematic errors when using inadequate models. Li et al.
(2021a) emphasized the importance of an optimal com-
promise between genome‐scale data and various models,
and increased the supports of several controversial nodes
within and among the classes of core Chlorophyta. Although
the taxon sampling in green algae has been recently ex-
panded, the sampling of clades with notable ecological and
morphological importance was still sparse. Future studies
with intensive taxon sampling and better‐fitting evolutionary
models, will greatly improve the resolution of the phyloge-
netic relationship of green algae.
Ecological and morphological diversification of early
green plants
Prasinophytes, the early diverging clades of the Chlorophyta,
predominantly flourishes in marine environments. The
Chlorophyceae and Trebouxiophyceae mainly thrive in
freshwater and terrestrial environments, and most algae from
Ulvophyceae have benthic marine habitats (Figure 1;Becker
and Marin, 2009;Leliaert et al., 2012). Based on the widely
accepted phylogeny of Chlorophyta, it is reasonable to hy-
pothesize that early green algae originated from marine en-
vironments, and later independently adapted to freshwater
and terrestrial environments (Li et al., 2021a). The transition
of habitats has shaped the cyto‐morphology diversification,
likely by driving the evolution of mechanisms underlying the
cell division. For instance, both Ulvophyceae and prasino-
phytes shared a similar type of microtubules‐mediated cy-
tokinesis and marine habitat, and the secondary loss of
phycoplast in Ulvophyceae likely resulted from the switch
back to marine habitats from freshwater habitats (Lewis and
McCourt, 2004;Del Cortona et al., 2020;Li et al., 2021a). It is
worth noting that the early branching green algae were al-
most unicellular, and multicellularity evolved independently in
different clades of green algae (Cocquyt et al., 2010;Del
Cortona et al., 2020;Li et al., 2021a). The transition from
unicellular to differentiated multicellular organisms was one
of the most important innovations in plant evolution, and it
marked an increase in the level of complexity of green plants.
Multicellularity has adaptive significance for green plants as it
has enabled adaptation to complex and changeable envi-
ronments, as well as laying the foundation for the differ-
entiation of tissues and organs in land plants (Umen, 2014).
The origin of early green plants and “Snowball Earth”
A reliable timescale of green plants provides a crucial
framework for understanding plant taxonomy, ecological di-
versity and interactions and co‐evolution with the global cli-
mate and various plant‐feeding organisms. Fossil records are
direct evidence in dating the divergence time of early green
plants. However, the algal fossils are largely acritarchs, and
their scarcity, fragmentation and uncertainty in taxonomic
affinities have largely hindered the accurate inference of the
origin time of green plants. For instance, Russian acritarchs
(~2,000−1,800 Ma) are taxonomically ambiguous, which
might be representatives of either Chlorophyta or Strepto-
phyta, or even a common ancestor of these two groups. This
acritarchs only assume that the common ancestor of Vir-
idiplantae and Rhodophyta have lived at least 2,000 Ma
(Teyssèdre, 2007). Although the recently discovered well‐
preserved fossils (Proterocladus antiquus) indicate that early
green plants, at least, have originated before 1,000 Ma, the
precise taxonomic affinities of Proterocladus remained con-
tentious (attributed to stem of Cladophorales or Ulvophy-
ceae) (Tang et al., 2020).
The surge in molecular data of green algae, the opti-
mization of the molecular clock model and improvements in
fossil calibration methods offer great potential for investigating
the origin time of green plants. Even with the improvements in
models and methods, considerable disparities have been
observed among the estimates of the divergence time of early
green plants (ranging from Paleoproterozoic to Neo-
proterozoic) (Heckman, 2001;Hedges et al., 2004;Zimmer
et al., 2007;Herron et al., 2009;Blank, 2013;Leliaert et al.,
2016;Morris et al., 2018). For instance, Blank (2013) employed
penalized likelihood and Bayesian methods, and inferred that
green plants originated at Paleoproterozoic (1,900−1,520 Ma).
Morris et al. (2018) applied the independent‐rates (IR) model
using large‐scale nuclear data and showed that green plants
occurred at Neoproterozoic (972−670 Ma). Recently, Nie et al.
(2020) took into account various sources of uncertainty,
such as different calibration strategies, clock‐partitioning
schemes, tree topology and evolutionary rate heterogeneity,
and collectively inferred that the early green plants
originated in the Paleoproterozoic to Mesoproterozoi (1,679.7
−1,025.6 Ma).
Interestingly, this origin time of early green plants is ap-
propriately earlier than the massive glaciation events
(“Snowball Earth”) in the Neoproterozoic era (Pierrehumbert
et al., 2011;Becker, 2013;Rooney et al., 2014;Prave et al.,
2016). The “Snowball Earth”hypotheses mainly have posited
geological explanations for Neoproterozoic glaciation
(Hoffman and Schrag, 2002;Goddéris et al., 2003;Rooney
et al., 2014). Nie et al. (2020) investigated the roles and
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mechanisms of green algae in shaping the global climate and
emphasized their potential impacts on the formation of gla-
ciers. Overall, the timeline of early green plants has laid the
groundwork for gaining further insights into the evolutionary
scenarios of green plants, as well as the history of global
climates and ecosystems.
STREPTOPHYTE ALGAE AND THE
ORIGIN OF LAND PLANTS
The phylogeny and morphological evolution of early
land plants
Much of our understanding of green plant evolution comes from
morphological and molecular evidence. However, the conflicts of
evolutionary trajectory inferred from molecular and morpho-
logical data still exist in green plants, especially in streptophyte
algaeandearlylandplants.Thesurgeingenomicdatahas
greatly alleviated the sparse gene and taxon sampling in recent
phylogenetic studies, and the branching order of streptophyte
algae and early land plants have been robustly resolved (Figure 2;
Puttick et al., 2018;de Sousa et al., 2019;One Thousand Plant
Transcriptomes Initiative, 2019;Su et al., 2021). The streptophyte
algae were paraphyletic and comprised the basal‐branching
Klebsormidiophyceae, Chlorokybophyceae, and Mesostig-
matophyceae(KCM)cladeandthehigher‐branching Zygnema-
tophyceae, Coleochaetophyceae, and Charophyceae (ZCC)
clade. The notion, Zygnematophyceae representing the most
likely sister group of land plants, was strengthened by multiple
phylogenomic analyses (Zhong et al., 2013,2014;Cheng et al.,
2019;One Thousand Plant Transcriptomes Initiative, 2019).
Bryophytes (liverworts, mosses and hornworts) were the
second‐most diverse group of land plants, and the rela-
tionships between bryophytes and tracheophytes have
been vigorously debated. Early cladistic studies using
morphological and biochemical characters, as well as the
mitochondrial multigene data, strongly supported the par-
aphyly hypothesis of bryophytes (Mishler and Churchill,
1985;Qiu et al., 2006;Qiu, 2008). The availability of large‐
scale nuclear genes and application of more complex
evolutionary models have shown that bryophytes formed
a monophyletic group, sister to the vascular plants
(Figure 2;Puttick et al., 2018;de Sousa et al., 2019;Su
et al., 2021;Donoghue et al., 2021). The inconsistent re-
lationships within bryophytes phylogeny is likely caused by
lineage‐specific differences of rate variation and deviating
amino acid/nucleotide composition. The widely accepted
notion that bryophyte is a monophyletic group was pro-
posed and strengthened by a series of phylogenomic
studies. Puttick et al. (2018) proposed the hypotheses that
bryophytes were monophyletic, and de Sousa et al. (2019)
further increased support for the monophyletic bryophytes
using the lineage‐heterogenous compositional model. Su
et al. (2021) recently yielded highly supported mono-
phyletic relationships of bryophytes by improving taxon
sampling of hornworts and eliminating the effect of syn-
onymous substitutions.
Reconstructing an accurate phylogeny of early land plants
attracts considerable interest in investigating the evolution of
morphological and developmental characters, especially the
innovative traits related to terrestrialization. The morpho-
logical characteristics of the early branching streptophytes
are simple (either Chlorokybophyceae or Meso-
stigmatophyceae from the KCM clade). The Klebsormidio-
phyceae diverged after Chlorokybophyceae and Meso-
stigmatophyceae, and evolved multicellularity, forming
packets of cells or simple filaments (Becker and Marin,
2009;Leliaert et al., 2016). The algae in higher‐branching
ZCC clade arising from the KCM clade at about 700 Ma, were
the first green plants to house more than one plastid per cell
(de Vries et al., 2016). Given that Zygnematophyceae are
recognized as the closest algal relatives to the ancestors of
land plants, their organismal complexity and lifestyles should
have high similarities with the early land plants. Surprisingly,
Zygnematophyceae have the least complex bodyplan of all
higher‐branching streptophyte algae, and they mainly are
unicellular and filamentous (Buschmann and Zachgo,
2016;Leliaert et al., 2019). It is worth mentioning that land
plants have inherited their genetic materials from the ances-
tral green algae, whereas their complex organs and tissues,
appears to have evolved on land. For example, comparative
genomic analyses of two early‐diverging subaerial/terrestrial
Zygnematophyceae revealed that many genes essential for
embryophytes are present in the common ancestor of Zyg-
nematophyceae and embryophytes (Cheng et al., 2019).
Nevertheless, various crucial traits (e.g., cuticle with stomata,
trilete spores and a basic body organization comprising
stems and reproductive structures) are unique features of
land plants (Gensel, 2008;Clarke et al., 2011).
The question is not only what the first land plants looked
like, but it is more interesting to figure out what contributes to
shape these features. It is well documented that the shift from
a haplobiontic life cycle with a single multicellular haploid
gametophytic generation (streptophyte algae) to a dip-
lobiontic life cycle (land plants), characterized by an alter-
nation of multicellular haploid and diploid generations, oc-
curred within green plants (Figure 2;Bowman et al.,
2016;Kenrick, 2017). Accordingly, it has been proposed that
the transition to land entailed changes in life cycle, and the
accompanied substantial somatic development resulted in
the evolution of tissues and organs basic to land plants, in-
cluding stems, leaves, roots, a vascular system, stomata, and
sex organs. Comparative analyses among chlorophyte algae
and land plants have pointed to the conservative evolutionary
history of the TALE‐class homeobox genes involved in reg-
ulating haploid‐to‐diploid transition in green plants (Bowman
et al., 2016;Horst et al., 2016). Variable gene expression has
been shown to help organisms to cope with multiple envi-
ronmental stresses in the short term, and it might also trigger
longer‐term adaptations during evolution by enhancing phe-
notypic variability and robustness (López‐Maury et al., 2008).
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Thus, the shifting of expression patterns of TALE homeobox
genes have been hypothesized to play important roles in
transforming plant life cycles. The process that recruiting and
integration of key traits evolved in distinct types of life cycles
was also critical for the adaptations to land of green plants.
For instance, stomata were thought to evolve in the spor-
ophytes with bryophyte‐like life cycles, facilitating spore
dispersal (Kenrick, 2017). Stomata has been co‐opted with
the gametophyte‐derived vasculature and rooting structures
in the most recent common ancestor of vascular plants,
laying the foundations of modern plant diversity (Duckett
et al., 2009).
It has been hypothesized that two consecutive bursts of
genomic novelty separately occurred in the ancestor of
streptophytes and the ancestor of land plants, likely con-
tributing to the origin of multicellularity and terrestrialization in
early land plants (Bowles et al., 2020). The bursts of genomic
novelty likely resulted from possible whole genome duplica-
tion (WGD) and horizontal gene transfer (HGT), which laid the
foundations of vital biological functions, including phyto-
hormone signaling, cell wall and root development, and
gravitropism. The molecular and physiological mechanisms
underpinning the innovations of bodyplan of land plants re-
main largely elusive despite extensive investigations, and
more systematic studies are urgently needed.
Timescale of land plants
Concerns over divergence time estimates for land plants
have attracted attentions of plant biologists and paleontolo-
gists, due to the time gap between molecular estimates and
fossil records. Macrofossils are typical land plants fossils,
and those from early land plants are very sparse. At present,
the oldest macrofossil came from a primitive vascular plant,
Cooksonia cf. Pertoni, suggesting that land plants occurred
at least in the Ludlow Silurian (426.9 Ma) (Edwards and
Feehan, 1980;Edwards et al., 1983). The discovery of fossil
spore assemblages provided new insights into the timescale
of early land plants (Edwards et al., 2014). Cryptospores with
permanent tetrads were regarded as spores of land plants
(Morris et al., 2018), and the well‐preserved cryptospores
(Tetrahedraletes cf. Medinensis) from the Dapingian Zanjon
Formation supported the origin time of land plants back to
469 Ma (Rubinstein et al., 2010).
Establishing a robust timescale requires using appro-
priate minimum and maximum constraints, and well‐dated
fossils only provide reliable minimum bounds. Maximum
calibration is usually constrained in two ways: (i) assigning
a parametric distribution on the age of the fossil (minimum)
calibration, such as the gamma, lognormal or the truncated
Gaussian distribution; (ii) assuming that a clade has not yet
evolved in a geologic period if there is an absence of fossils
in that period, in which case the upper bound of the period
is the maximum constraint for the clade. The maximum
constraint for crown land plants has been controversial,
and different divergence times of land plants have been
obtained using various maximum bounds (Clarke et al.,
2011;Hedges et al., 2018;Morris et al., 2018;Su et al.,
2021). Employing the maximum age of the oldest‐possible
non‐marine palynomorphs (515 Ma) as the maximum
bound appeared to constrain the origin time of land plants
within the narrow time interval, from Middle Cambrian to
Early Ordovician (515−470 Ma) (Morris et al., 2018). This
strategy largely amplified the effects of maximum bound
and ignored the contribution of molecular data in time es-
timation, resulting in a relative younger origin.
Interestingly, when removing the maximum constraint,
or using the more conservative time of 1 042 Ma (repre-
senting a sampled Precambrian locality yielding no plant‐
like spores), the origin time of land plants have been es-
timated as much older (793−560 Ma (Hedges et al., 2018);
815−568 Ma (Clarke et al., 2011)). Su et al. (2021)inves-
tigated the impacts of different maximum bounds on
the origin of land plants and assumed a Precambrian
(980−682 Ma) origin for land plants by considering the
reliability of fossil calibrations and the influenceofmo-
lecular data. More importantly, Su et al. (2021)claimed
that fossil calibrations used to estimate the timescale of
plant evolution need more scrutiny, and the important
contribution of molecular data (time‐dependent molecular
changes) should be valued when faced with controversial
fossil evidence. Intriguingly, the recent discovery of a
fossil spore assemblage has documented an Early Ordo-
vician (480 Ma) origin of land plants, closing the gap be-
tween molecular and fossil estimates and supporting an
earlier origination of land plants (Strother and Foster,
2021). The high potential for fossil preservation of bryo-
phyte material has raised the possibility of many exquisite
fossils of early land plants (Tomescu et al., 2018), which
could provide novel information for exploring the timeline
of land plants and bring fossils and molecular estimates
into a closer alignment.
DARWIN'S “ABOMINABLE
MYSTERY”IN ANGIOSPERMAE
Complex evolutionary routes of angiosperms
Angiosperms (flowering plants) are the most successful
groups, exhibiting extensive morphological and ecological
diversity, and have great advantages in modern terrestrial
ecosystems. The angiosperm phylogeny has been greatly
improved in the last two decades (Chase et al., 1993;Soltis
et al., 1999,2011;Moore et al., 2007,2010;Qiu et al.,
2010;Ruhfel et al., 2014;Wickett et al., 2014;Zeng et al.,
2014;Group et al., 2016;Zhong and Betancur‐R, 2017;
Gitzendanner et al., 2018;Givnish et al., 2018;One Thousand
Plant Transcriptomes Initiative, 2019;Li et al., 2019). Most
studies supported the Amborella‐sister hypothesis that Am-
borella was the earliest diverging lineage of angiosperms,
followed successively by Nymphaeales and Austrobaileyales
(Figure 2;Albert et al., 2013;Drew et al., 2014;Zhong and
Betancur‐R, 2017;One Thousand Plant Transcriptomes
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Initiative, 2019;Zhang et al., 2020a). Particularly, early
studies have questioned the basal position of Amborella, and
regarded it as a phylogenetic artifact caused by long‐branch
attraction and poor fit between evolutionary models and se-
quence data (Xi et al., 2014;Goremykin et al., 2013,2015).
Recent phylogenomic analyses with expanded taxon sam-
pling supported the Amborella‐sister hypothesis, by amelio-
rating potential systematic errors which arose from limited
taxon sampling and gene tree estimation error (Zhong and
Betancur‐R, 2017;One Thousand Plant Transcriptomes Ini-
tiative, 2019;Li et al., 2021b). More attention should be paid
to alleviate the effects of poor fit between evolutionary
models and sequence data, and explore the relative con-
tribution of biological factors (e.g., incomplete lineage sorting
(ILS), hybridization and gene duplication/loss) to phyloge-
netic incongruence.
The remaining angiosperms form a monophyletic clade,
Mesangiospermae, which is subdivided into five major
groups: eudicots, monocots, magnoliids, Chloranthales, and
Ceratophyllales. Numerous phylogenomic studies using
large‐scale nuclear genes supported monocots as sister to
the rest of Mesangiospermae, whereas the branching order
of four remaining clades varied among different analyses
(Figure 2). One Thousand Plant Transcriptomes Initiative
(2019) supported that eudicots+Ceratophyllales were sister
to Magnoliids+Chloranthales, which has been recently con-
firmed by genomic data (Guo et al., 2021;Ma et al., 2021).
However, few studies have recovered alternative topologies
among these clades (Zeng et al., 2014;Yang et al., 2020a).
For example, Zeng et al. (2014) reported that eudicots were
sister to Ceratophyllales+Chloranthales, which were in turn
sister to Magnoliids. Meanwhile, the chloroplast phyloge-
nomic analyses received topologies that magnoliids and
Chloranthales were the successive sister to other Me-
sangiospermae lineages (Li et al., 2019,2021b), or the clade
of Magnoliids and Chloranthales was sister to other Me-
sangiospermae lineages (Moore et al., 2007,2010;Soltis
et al., 2011;Ruhfel et al., 2014;Gitzendanner et al., 2018).
The discordance between nuclear and organellar phyloge-
nies has been widely observed at the deep levels of angio-
sperm phylogeny, especially in the placement of monocots,
Magnoliids and Chloranthales (Soltis et al., 2011;Ruhfel
et al., 2014;Zeng et al., 2017;Gitzendanner et al., 2018;
Li et al., 2019;One Thousand Plant Transcriptomes
Initiative, 2019).
Current studies mainly focused on dense taxon and gene
sampling to reconstruct the angiosperm phylogeny, whereas
few explicitly investigated the cause of phylogenetic conflicts
in the backbone of angiosperm phylogeny (Yang et al.,
2020a,2020b;Guo et al., 2021;Ma et al., 2021). The cyto-
nuclear discordance and incongruence among nuclear gene
trees have been documented as the consequence of several
evolutionary processes, including ILS, gene duplication and
loss, and gene flow (hybridization and introgression). The
recent phylogenomic analyses have identified that both hy-
bridization and ILS together contributed to these
discordances in the backbone of angiosperm phylogeny
(Guo et al., 2021;Ma et al., 2021).
Duetothesimilarpatternsofphylogenetic discordance pro-
duced by both processes, it appears to be difficult to exactly
distinguish hybridization from ILS. The relative contribution of ILS
or hybridization to phylogenetic conflicts also has not been
carefully evaluated. Assessing the relative influence of these two
processes would greatly enhance our understanding of the
evolutionary forces driving rapid radiation of angiosperms. More
importantly, Yang et al. (2020a) uncovered that the polytomy
among five major lineages of Mesangiospermae could not be
rejected, implying that a strictly bifurcating tree might not ad-
equately represent early radiation of angiosperms. Detecting the
patterns of reticulation in the backbone of angiosperm phylogeny
would allow for a more thorough understanding of the evolution
of angiosperms.
The origin time of angiosperms and “Jurassic gap”
Compared with green algae and early land plants, the fossils
of seed plants are abundant and relatively reliable. As the
early branching seed plants, gymnosperms form a small
monophyletic group, comprising about 800 species (http://
www.mobot.org/MOBOT/research/APweb/), and gymno-
sperms and angiosperms have diverged in the Carboniferous
(359−299 Ma) (Won and Renner, 2006). The first radiation of
angiosperms occurred in the early Cretaceous; however, few
reliable fossil records of angiosperms have been found in
strata prior to the Early Cretaceous (Herendeen et al., 2017).
Although many older fossils have been reported, most of
them cannot stand up to scrutiny. For instance, Liaoning-
fructus ascidiatus, an early Cretaceous Yixian Formation
fossil found in Liaoning, was once thought to be an angio-
sperm (Wang and Han, 2011). However, this fossil has now
been reassessed as a conifer, as the initially interpreted
structure, the fruit with ascidiate carpels containing two
seeds is actually galls on the linear leaves of the conifer
(Liaoningocladus)(
Wong et al., 2015). Similarly, fossils of
Euanthus panii and Aegianthus daohugensis from the Ju-
rassic have been carefully re‐examined, and the evidence for
them claimed as angiosperms was either weak or non-
existent (Krassilov and Bugdaeva, 1988,1999;Zheng and
Wang, 2010;Deng et al., 2014;Liu and Wang, 2016;
Herendeen et al., 2017). At present, the pollen fossils (espe-
cially the tricolpate pollen fossils) found in the Early Creta-
ceous (~133–125 Ma) were widely accepted as angiosperm
fossil records (Barremian‐Aptian transition), which could be
reliably assigned as crown‐group angiosperms (Hughes and
McDougall, 1990;Hughes, 1994). However, most molecular
clock studies indicated that angiosperms began to diverge
into modern groups at Jurassic or even earlier, suggesting
the “Jurassic gap”between the fossil records and molecular
clock estimates (Smith et al., 2010;Clarke et al., 2011;Zeng
et al., 2014;Beaulieu et al., 2015;Barba‐Montoya et al.,
2018;Li et al., 2019;Yang et al., 2020a).
In recent years, many studies have been devoted to
explaining this temporal difference from various
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perspectives. Through a series of simulations, Beaulieu
et al. (2015) demonstrated that the potential biases
caused by rate heterogeneity between herbaceous and
woody species tended to generate the older age esti-
mates, especially large shifts in branch rates among early‐
diverging lineages of angiosperms. Recent studies have
revealed contrasting results, suggesting that rate hetero-
geneity had little effect on the age of crown angiosperms
(Foster et al., 2017;Yang et al., 2020a). Given the im-
portant contribution of phylogenetic information in Baye-
sian dating analyses, Brown and Smith (2018) highlighted
that the configuration of statistical inference problems
(e.g., parameters, relationships and associated priors)
might hinder the inference of the crown age of angio-
sperms. Various molecular dating analyses all supported
apre‐Cretaceous angiosperm origin by expanding taxon
sampling and nuclear genes, and by considering the ef-
fects of different variables in the molecular clock (Barba‐
Montoya et al., 2018;Li et al., 2019;Yang et al., 2020a).
The time gap between molecular data and fossil evidence
was a typical problem (Nel et al., 2013;Misof et al., 2014),
and recent advances in palaeobotanical records have
narrowed the “Jurassic gap”.Shietal.(
2021)discovered
the early Cretaceous fossil assemblage in Inner Mongolia,
and supported that the ancestral taxa of angiosperms
emerged in the Triassic about 250 Ma, likely implying the
pre‐Cretaceous origin of angiosperms. Future discoveries
of reliable fossils are needed to unravel the mysteries of
the “Jurassic gap”.
THE EVOLUTION OF LIGHT
SENSING AND SIGNALING IN
GREEN PLANTS
What physiological properties allow the first land plants to
thrive? Light is undoubtedly a predominant environmental
factor, and green plants have evolved complex light per-
ception and transduction pathways to immediately adjust
their physiological responses, balancing the growth, devel-
opments and stress response.
Cryptochromes and phototropins: Catching the first
flash of light in the deep sea
Light, one of the most influential environmental factors during
the life cycle of plants, not only fuels the plants through
photosynthesis, but supplies critical cues of environments to
mediate their growth and developments, such as diurnal
rhythm and neighboring plants. The wavelength, intensity and
composition of light drastically change from deep sea to
water surface, from aquatic environment to dry land (Maberly,
2014;Han et al., 2019). In response to corresponding light
signal variation, green plants have evolved different light
sensory systems for light signal perception and transduction.
From the origin of Archaeplastida, most ancient plants lived
in the deep sea, and only utilized blue light as the main
energy and signal source, due to the absorption of UV‐B and
red/far‐red light by water (Figure 3;Singh et al., 2015).
Cryptochrome is the well documented blue light photo-
receptor in plants, and it belongs to the cryptochrome/photo-
lyases superfamily that highly diversified throughout the eukar-
yotes (Losi and Gärtner, 2012;Fortunato et al., 2015). Both
cryptochrome and photolyases have the conserved DNA pho-
tolyase and flavin adenine dinucleotide (FAD) binding domains,
whereas plant cryptochromes possess a cry carboxyterminal
extension (CCT), which is essential for mediating the light sig-
naling (Liuetal.,2011,2017;Zuo et al., 2011). Cryptochromes
could absorb different light through the binding of chromo-
phores, including FAD for UV‐A and the light‐harvesting deaza-
flavin or pterin like 5,10‐methenyltetrahydrofolate (MTHF) for blue
light (Falciatore and Bowler, 2005). In green plants, light could
activate the nuclear‐localized cryptochromes to homodimerize
and bind to downstream signaling components, regulating the
hypocotyl elongation, flowering and the circadian clock (Franklin
et al., 2014;Christie et al., 2015).
Phototropins (PHOTs) are also the blue‐light receptors that
originated in green plants. PHOTs control a series of photo-
synthetic efficiency optimization in land plants, including photo-
tropism, light‐induced stomatal opening, and chloroplast move-
ments in light intensity changing process (Christie, 2007). In the
model alga Chlamydomonas reinhardtii, photoactivated PHOT
could cause changes of expression levels of specific targets and
was essential for its sexual life cycle completion and acclimation
to high‐light stress (Huang and Beck, 2003;Aihara et al., 2019).
Previous studies have shown that PHOTs only presented in all
major clades of green plants, and were absent in glaucophytes,
rhodophytes, cryptophytes, haptophytes, or stramenopiles, in-
dicating that PHOTs originated within green plants (Li et al.,
2015a;Li and Mathews, 2016). Thus, it is reasonable to presume
that the evolution of blue light signaling pathway provided the
opportunity to sense and utilize the light in deep sea, facilitating
their survival and laying the foundations for subsequent terres-
trialization.
UV RESISTANCE LOCUS 8 (UVR8): the sentinels of
UV‐B radiation in shallow water
During the transition from deep sea to shallow water, green algae
evolved the UV‐B signaling pathways, allowing them to survive
the high UV‐B irradiation in shallow water (Figure 3;Li and
Mathews, 2016;Aihara et al., 2019). High UV‐B irradiation con-
stitutes a potential abiotic stress factor for photosynthetic plants
with sessile lifestyle, whereas low dose rates of UV‐B act as a
signal to regulate plant photomorphogenesis and induce UV‐B
acclimation (Frohnmeyer and Staiger, 2003). UVR8 has been
characterized as the exclusive UV‐B photoreceptor in green
plants, and could sense UV‐B radiation via intrinsic tryptophan
residues functioning as chromophores (Wu et al., 2012;Tilbrook
et al., 2016;Tossi et al., 2019). Phylogenetic studies indicated
that UVR8 is a specificUV‐B receptor and widely exists in most
clades of green plants (Fernández et al., 2016;Han et al., 2019).
There have been two different types of UVR8‐mediated signaling
pathways: (1) the canonical UVR8‐COP1/SPA‐HY5‐RUP
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signaling pathway; (2) the direct binding of UVR8 to specific
transcription factors (TFs) (Liang et al., 2018;Yang et al.,
2018,2020c). Zhang et al. (2021) recently discovered that the
canonical UVR8‐COP1/SPA‐HY5‐RUP signaling pathway origi-
nated in chlorophytes, and the interactions between UVR8 and
downstream TFs mainly originated in charophytes and early land
plants. Moreover, the binding of UVR8 to specific TFs confers the
cross‐talks between environmental UV‐B signal and hormonal
signal in green plants, likely expanding the repertoires of UV‐B
signaling pathway. Multiple UVR8‐mediated signaling pathways
ensure UV‐B signal transduction and physiological response,
reflecting the adaptations of green plants to the UV‐Bradiation
during terrestrialization.
Phytochromes: the last step before slogging on land
During the adaptations to the subaerial/terrestrial habitats,
charophytes employ the phytochrome signaling pathway for
acquiring red/far‐red light (600–750 nm) as the main energy
source and crucial light signal (Figure 3). Plant phytochromes
(encoded by PHYA‐PHYE) have been classified into two
types: (i) phyA is the only type I phytochrome (photo‐labile);
(ii) phyB‐E are type II phytochromes (photo‐stable) (Quail,
1997;Li et al., 2015b;Rockwell and Lagarias, 2020). Phyto-
chromes generally occur in two reversible conformations: Pr
and Pfr, which could separately transit through red and far‐
red light absorption, mediating the nucleus translocation and
contributing to the light responses and development (Franklin
and Quail, 2009;Strasser et al., 2010;Rausenberger et al.,
2011;Ádám et al., 2013;Hu et al., 2013;Klose et al.,
2015;Sánchez‐Lamas et al., 2016). Plant phytochromes
usually contain two modules, the photosensory module in N‐
terminal of phytochromes including a Period/Arnt/Single‐
Minded (PAS) domain, a cGMP phosphodiesterase/adenylyl
cyclase/FhlA (GAF) domain, and a phytochrome‐specific
(PHY) domain; the output module in C‐terminal with two
tandem PAS domains termed PRD (PAS‐repeat domain) and
a histidine kinase‐related domain (HKRD) (Krall and Reed,
2000;Nagatani, 2010).
In the past years, the origin and evolution of the phyto-
chrome signaling pathway have been well‐studied. Canonical
Figure 3. The origin and evolution of the light signaling network in green plants
Light conditions vary along different environmental niches of green plants. In deep sea, red/far‐red light and UV‐B are mostly absorbed, and thus most red
algae use blue light as the main light signal and energy source; blue light receptors and main components of corresponding signaling pathway originatein
this period. During the transition from deep sea to shallow water, green algae evolve the UV‐B signaling pathway (UVR8 and other important signaling
components), allowing them to survive the high UV‐B irradiation in shallow water. To adapt to the subaerial/terrestrial habitats, charophytes employ the
phytochrome signaling pathway for utilizing red/far‐red light as the principal signal and energy source, preparing for the conquering of land. Land plants
evolve a series of fine‐tuning downstream regulators for transducing various light signals on land, such as FHY1, FHY3 and LAF1, and eventually establish
the elaborate light signaling network in angiosperms.
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phytochromes (plant phytochromes) have been widely iden-
tified in streptophytes, confirming the charophyte origin of
the canonical phytochrome (Li et al., 2015b;Li and Mathews,
2016). In contrast, the non‐canonical phytochrome com-
prised various types, and widely existed in glaucophytes,
chlorophytes, fungi and bacteria (Rockwell and Lagarias,
2020). Rather than origination through endosymbiotic gene
transfer (EGT), several studies supported that multiple HGT
events gave rise to extant eukaryotic phytochromes (Li et al.,
2015b). Importantly, the fusion among phytochrome and
other different photoreceptors is a vital mechanism, driving
its adaptation and evolution. Dualchrome1 (DUC1) and neo-
chromes were discovered as chimeric photoreceptors.
DUC1, consisting of a two‐domain fusion of PHY and CRY,
originated from a prasinophyte alga, Pycnococcus provasolii
(Makita et al., 2021). Neochromes were fused by PHY and
PHOT, which were mostly discovered in ferns (Nozue et al.,
1998;Kawai et al., 2003;Suetsugu et al., 2005). The photo-
receptor chimera provides more efficient utilization of light in
ferns and algae, and these discoveries raise interesting
questions about the evolution of these photoreceptor fami-
lies. Not only phytochromes have experienced various in-
novations, but more regulatory genes also evolved to fine‐
tune the light regulatory networks for complicated terrestrial
environments (Rensing, 2018).
COP1‐SPA: The heart of light signaling networks
COP1 forms an E3 ubiquitin ligase complex together with the
four SPAs (SPA1‐4), and COP1‐SPA complex directs
photomorphogenesis‐promoting factors to be degraded
through the 26S proteasome system, resulting in the re-
pression of photomorphogenesis in the dark (Lian et al.,
2011;Liu et al., 2011;Zuo et al., 2011;Lu et al., 2015;Sheerin
et al., 2015;Balcerowicz et al., 2017;Podolec et al., 2021).
Both COP1 and SPAs have the highly similar domains, in-
cluding a middle coiled‐coil domain and C‐terminal WD40
repeats, whereas COP1 possesses an additional N‐terminal
kinase‐like domain (Deng and Quail, 1992;Deng and Matsui,
Wei, et al., 1992;Stoop‐Myer et al., 1999;Holm et al.,
2001;Menon et al., 2016). Photoactivated photoreceptors
could interact with the WD40 domain of COP1 via their VP
domains (cryptochromes and UVR8, sometimes phosphory-
lated), repressing its E3 ligase activity and releasing its sub-
strates for downstream signaling transduction (Osterlund
et al., 2000a,2000b;Lau and Deng, 2012;Lau et al., 2019). It
has been reported that COP1 originated in the common an-
cestor of all eukaryotes (Han et al., 2020), whereas SPAs
were plant‐specific proteins, originating in chlorophytes
(Figure 3;Xu et al., 2021). These studies indicated that the
interactions between SPAs and COP1 originated at least in
early land plants, and SPAs likely experienced sub-
functionalization/neofunctionalization after its divergence in
the ancestor of euphyllophytes (ferns and seed plants) (Xu
et al., 2021). COP1/SPA complexes serve as the central re-
pressor in multiple light signaling pathways, and activated
photoreceptors can repress their functions (Kang et al.,
2009;Jeong et al., 2010). Although the sequence and func-
tion of COP1 is highly conserved in plants and animals, SPA
and COP1/SPA complex formation are plant specific. COP1
and SPA have shown significant codivergence and strong
coevolution signals in angiosperms (Han et al., 2019). The
expansion of COP1 and SPA gene families in angiosperms
might have promoted the formation of various COP1/SPA
complexes for response to different light conditions on land
(Laubinger et al., 2004;Han et al., 2019;Xu et al., 2021).
Although cryptochromes and COP1 already existed in the
ancestor of plants, the co‐evolution and optimization of light
perception and downstream signal transduction components
evidently contributed to the plant terrestrialization. The
UVR8‐mediated signaling pathways enabled plants to deal
with UV‐B in shallow water, and the phytochrome signaling
pathway helped plants to colonize the subaerial/terrestrial
habitats. Acclimation to different distributions of light quality
in new environments resulted in the origination and evolution
of specific light signaling pathways, ultimately contributing to
the complex light signaling networks in green plants.
THE INNOVATIONS OF GENETIC
VARIATION IN GREEN PLANTS
The extent and role of HGT in the evolution of green
plants
The process of genetic movement between species is re-
ferred to as horizontal or lateral gene transfer (HGT or LGT).
HGT has long been regarded as a crucial evolutionary force
that drives the adaptations and diversities of prokaryotes
(Peter et al., 2002;Soucy et al., 2015), whereas more atten-
tion has been devoted to investigating the HGT events from
bacteria/fungi to green plants with the increasing of genomic
data. The well‐known HGT event was the endosymbiotic
gene transfer of cyanobacterial genes into the eukaryotic
host nuclear genome (Timmis et al., 2004), resulting in the
ancient photosynthetic eukaryotes. The acquisition of pho-
tosynthetic ability from the acquired plastid had far‐reaching
consequences for plant evolution, not only relieving the het-
erotrophic host from the dependency on the continuous up-
take of organic carbon, but conferring them the assimilating
and metabolic functions of some organic/inorganic elements
(Weber and Flügge, 2002;Balk and Lobréaux, 2005;Wang
and Benning, 2012).
The acquisitions of novel genes through HGT in green
plants have been widely documented, and these HGT‐
derived genes are involved in various biological process,
including DNA damage repair, starch metabolism, plant
defense and environmental stress response (Figure 4;Yue
et al., 2012;Soucy et al., 2015;Hirooka et al., 2017;Zhang
et al., 2020b). Especially, it has been shown that many HGT
events occurred in charophytes and bryophytes, due to the
spatial proximity between them and soil bacteria/fungi,
likely facilitating the generation of innovative traits related
to terrestrialization. For example, the common ancestor of
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Zygnematophyceae and embryophytes have presumably
acquired the PYR/PYL/RCAR and GRAS gene families from
the soil bacteria through HGT, and they could separately
encode abscisic acid (ABA) receptors and essential
regulators of plant growth and development (Cheng et al.,
2019). The transaldolase (TAL)‐type gene has been identi-
fied as an HGT‐derived gene in the ancestor of strepto-
phytes from bacteria, and transgenic experiments showed
Figure 4. The widespread whole genome duplications (WGDs) and putative horizontal gene transfers (HGTs) in green plants
The green plant phylogeny is based on One Thousand Plant Transcriptomes Initiative (2019). The red dots represent the putative WGDs inferred by Wood
et al. (2009), Devos et al. (2016), Ren et al. (2018), One Thousand Plant Transcriptomes Initiative (2019), Gao et al. (2020), Huang et al. (2020), Silva et al.
(2021) and Stull et al. (2021). The putative HGT events and their potential functions of HGT‐derived genes in green plants are shown. Black dotted line
indicates the transfer of genes associated with starch metabolism from bacteria to green plants (Yue et al., 2012;Soucy et al., 2015). Green and red dotted
lines separately indicate the transfer of genes related to the development and stress response from bacteria to chlorophytes and charophytes (Yue et al.,
2012,Yang et al., 2015b;Hirooka et al., 2017,Cheng et al., 2019,Zhang et al., 2020b,Chen et al., 2021). Yellow dotted line indicates the transfer of genes
involved in DNA damage repair from bacteria to mosses (Yue et al., 2012;Soucy et al., 2015).
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that knock‐down of TAL in rice could result in smaller and
immature vascular bundles, implying the vital role of TAL in
plant vascular system development (Yang et al.,
2015b;Chen et al., 2021).
It is no doubt that HGTs have occurred in some lineages
of green plants, but the extent and role of HGTs in the evo-
lution of green plants appear to be overstated for various
reasons. The plant genomic data has shown great advan-
tages in identifying HGT‐derived genes, whereas it also has
amplified the potential false positives. The HGT‐derived
genes in green plants were identified based on a combina-
tion of sequence similarity searching and phylogenetic tree
reconstruction. This method is proved to be effective in
identifying HGT events among distantly related species (such
as between bacteria/fungi and green plants), but we should
be cautious to apply this to closely related species. Multiple
processes (e.g., introgression, gene duplication/loss and ILS)
of gene evolution might produce similar tree topology, thus
misleading us in assessing the extent of HGTs in green
plants. Another important factor of possible false positivity
was from genome contamination. Although the genome se-
quencing, assembly, and annotation approaches have been
greatly developed, the contaminations in plant genomes were
still a non‐negligible issue due to the complex living con-
ditions and lifestyles of plants.
It has been shown that the transferred genes were nearly
neutral or at least harmless for the recipients (Gogarten and
Townsend, 2005;Soucy et al., 2015). The HGT‐derived genes
might be recruited and experienced natural selection during
evolution, resulting in the stable inheritance or loss of the
transferred genes (Soucy et al., 2015). It was an exemplar
case that plants evolved the capacity to produce toxins for
defense, and plant‐feeding insects acquire corresponding
genes for detoxification through HGTs, representing a typical
example of “arms race”driven by HGTs (Li et al., 2011;Xia
et al., 2021). Nevertheless, the biological function of most
identified HGT‐derived genes in green plants were largely
unknown, which has limited the investigation of their sig-
nificance in plant adaptation and evolution. Future work
should strive to improve the methods for identifying HGT,
investigate the mechanisms underpinning HGT, and explore
the evidences that evaluate the significance of HGT events.
Extensive WGDs in land plants
Whole‐genome duplication, or polyploidy, has long been
recognized as a ubiquitous phenomenon during land plant
evolution. Numerous studies have implicated that recent and
ancient polyploidization events occurred repeatedly
throughout all the major land plant lineages, with the most
frequency of WGD in angiosperms (Figure 4;Jiao et al.,
2011,2014;Li et al., 2015c;Ren et al., 2018;One Thousand
Plant Transcriptomes Initiative, 2019;Huang et al., 2020;Wu
et al., 2020;Zhang et al., 2020c;Stull et al., 2021). Ancient
polyploidy in the ancestry of angiosperms and seed plants
has been identified (Jiao et al., 2011), and over 180 WGDs
have been further reported in all extant angiosperm lineages
(One Thousand Plant Transcriptomes Initiative, 2019). Among
other plant lineages, 31% of the speciation events in ferns
were reported to be associated with genome duplication
(Wood et al., 2009), and three ancient WGDs were identified
along the phylogenetic backbone of ferns (Huang et al.,
2020). Recent studies have revealed that the mosses Syn-
trichia caninervis and Physcomitrella patens shared an an-
cient WGD, and multiple ancient large‐scale duplication
events occurred in the ancestor of the bryophytes (Devos
et al., 2016;Gao et al., 2020;Silva et al., 2021). Compared to
the extensive WGD in land plants, the evidence of WGD was
exclusively found in the early diverging Zygnematophyceae
(Spirogloea muscicola)(
Cheng et al., 2019).
Although many polyploidy events have been documented
throughout plant evolution, our knowledge about their evo-
lutionary consequences and impacts on plant ecology are
limited. Previous studies have shown that numerous WGDs
were not randomly distributed over time, but rather correlated
with periods of extinction or dramatic global change (Levin
and Soltis, 2018;Wu et al., 2020;Koenen et al., 2021;Silva
et al., 2021;Van de Peer et al., 2021). Multiple independent
WGDs occurred around the Cretaceous‐Paleocene (K‐Pg)
boundary, implying the possible roles of WGDs in con-
tributing to the survival of species during the extinction event
(Vanneste et al., 2014;Wu et al., 2020). Recent evidence has
indicated that gene families that contribute to adaptations to
specific environmental changes were co‐retained duplicates
from a wave of independent polyploidy events, such as
global cooling and darkness during the K‐Pg boundary (Wu
et al., 2020). This study also demonstrated that different
families of TFs showed certain preferences of retention, and
key members in stress‐related networks commonly pre-
sented as high‐retention after multiple independent WGDs.
Analyses of ancient gene duplications in mosses have sug-
gested that recurrent significant retention of stress‐related
genes might have contributed to their adaptations to distinct
ecological environments (Gao et al., 2020). Moreover, Soltis
et al. (2015) have proposed that WGD might lead to a ge-
nomic combination for the origin of evolutionary novelty, re-
sulting in a burst of diversification of green plants. Indeed,
many WGDs in green plants were proved to facilitate the
increase of species diversification rates. For example, Huang
et al. (2020) demonstrated that three WGDs along the back-
bone of fern phylogeny were positively correlated with their
diversification rate shifts. Landis et al. (2018) revealed that 61
of 106 WGD events were associated with shifts in diversifi-
cation rates across angiosperm phylogeny, and these WGD
events appeared to occur within a period of environmental
instability.
Ancient WGDs were crucial driving forces that shaped
the origin of key innovations during plant evolution, es-
pecially in angiosperms. The ancient WGDs which oc-
curred in early evolution of angiosperms were likely to be
responsible for several structural innovations of flowers,
and most notable innovations were the developments of
sealed carpel and true vessel elements in stem tissue
Evolutionary history of green plantsJournal of Integrative Plant Biology
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(Carlquist and Schneider, 2002;Soltis et al., 2009;Soltis
and Soltis, 2016). Another example was the rapid di-
versification of glucosinolate compounds in the Brassi-
cales. It has been demonstrated that most genes in the
glucosinolate pathway were derived from WGDs in the
history of Cleomaceae and Brassicaceae (Bergh et al.,
2016). The diversification of glucosinolate compounds
that was facilitated by neofunctionalization of these du-
plicate genes have contributed to the “arms race”be-
tween plants and herbivores, influencing the terrestrial
ecosystems (Edger et al., 2015). The understanding of
connections and mechanisms among WGDs, radiation,
origin of innovative traits and adaptations still needed
future studies to advance our understanding of them.
CONCLUSIONS AND
PERSPECTIVES
In the past two decades, the phylogenetic resolution of
green plants has been greatly improved with the growing
wealth of genomic data from increasingly diverse sets of
species. However, there are several important aspects that
we need to consider in future studies, such as the poor fit
between evolutionary models and molecular data, identi-
fying and assessing the biological factors in phylogenetic
inference, and the “time gap”between molecular estimates
and fossil records. Evolutionary biologists have been de-
voted to enhance the biological realism of evolutionary
models that introduce enormous computational burdens.
The field of computing science is growing rapidly, and the
improvements in computing capabilities greatly relieve the
limitation of applying complex/realistic models in phylo-
genomics. Importantly, it is necessary for plant biologists
to investigate the morphological and physiological traits in
the light of evolution, and understand their genetic mech-
anisms and biological functions into an evolutionary
context.
Although various innovative traits have been identified in
green plants, researchers still lack comprehensive under-
standing of their functions, limiting the establishments of
connections between phenotypic novelties and adaptive
evolution. Key differences in adaptive diversification are likely
concerning complicated physiological processes, such as
root systems, organismal architectures and reproductive bi-
ology. The development of increasingly sophisticated omics
technologies (e.g., genomics, transcriptomics and proteo-
mics) provides a means of gaining more insight into the
physiologies of these trait differences. Omics approaches are
useful for exploring the non‐model organisms with crucial
phylogenetic positions or thriving in harsh environments,
providing a glimpse of the molecular mechanisms related to
plant adaptations. However, the knowledge gaps among
omics analyses and gene functions and actual regulatory
networks need further wet‐lab experiments in order to
fill them.
ACKNOWLEDGEMENTS
We greatly appreciate Hongzhi Kong for valuable comments,
and three anonymous reviewers’critical reading that helped
improve the manuscript. We sincerely apologize to re-
searchers whose studies were not included in this review
owing to space constraints. This work is supported by the
National Natural Science Foundation of China (32122010,
31970229 and 32100178), the Collaborative Innovation
Center for Modern Crop Production co‐sponsored by Prov-
ince and Ministry, and the Priority Academic Program De-
velopment of Jiangsu Higher Education Institutions (PAPD).
CONFLICTS OF INTEREST
The authors declare they have no conflicts of interest asso-
ciated with this work.
AUTHOR CONTRIBUTIONS
B.Z. conceived the project and designed the review; Z.Z., X.
M., Y.L., L.Y., X.S., H.W., and R.D. wrote the manuscript. All
authors reviewed and approved of the manuscript.
Edited by: Zhizhong Gong, China Agricultural University, China
Received Oct. 23, 2021; Accepted Jan. 8, 2022; Published Jan. 12, 2022
FA: Free Access
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