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Journal of Integrative Invited Expert Review
JIPB Plant Biology 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 ([email protected])

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
are three key evolutionary events during the
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,
Zhenhua Zhang Bojian Zhong 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
ABSTRACT of green plants. Ultimately, we highlight funda-
Green plants (Viridiplantae) are ancient photo- mental questions to advance our understanding
synthetic organisms that thrive both in aquatic of the phenotypic novelty, environmental
and terrestrial ecosystems, greatly contributing adaptation, and domestication of green plants.
to the changes in global climates and ecosys- Keywords: adaptation, divergence times, green plants, key
tems. Significant progress has been made to- innovations, phylogenetics, terrestrialization
ward understanding the origin and evolution of Zhang, Z., Ma, X., Liu, Y., Yang, L., Shi, X., Wang, H., Diao, R.,
green plants, and plant biologists have arrived and Zhong, B. (2022). Origin and evolution of green plants in the
at the consensus that green plants first light of key evolutionary events. J. Integr. Plant Biol. 64: 516–535.

INTRODUCTION eukaryote (Dagan et al., 2013; de Vries et al., 2016; Leliaert

et al., 2019).

T he primary endosymbiotic event gave rise to three pho-

tosynthetic lineages, including green plants (Vir-
idiplantae), red algae (Rhodophyta) and Glaucophyta, which
Green plants are the major groups of oxygenic photo-
synthetic eukaryotes, including green algae and their de-
scendants: streptophyte algae (charophytes) and land plants
together formed the Archaeplastida. Over millions of years of (embryophytes) (Leliaert et al., 2012). Green algae include
evolution, multiple lineages of the ancient photosynthetic two major groups: Chlorophyta, the well‐documented ancient
eukaryotes have successfully adapted to terrestrial environ- photosynthetic eukaryotes; and Prasinodermophyta, a novel
ments (Raven and Edwards, 2014). Among these organisms, phylum that diverged before the split of Chlorophyta and
green plants are the most successful group, and show Streptophyta (Figure 1; Leliaert et al., 2016; Li et al., 2020).
high biodiversity and wide distribution in subaerial/terrestrial Green algae are not only of particularly evolutionary interest
habitats, comprising ~450,000−500,000 species (Guiry, due to their high morphological and cytological diversity, but
2012; Corlett, 2016). Green plants originated from the primary also their great contribution to the global ecosystem
endosymbiotic event, which probably took place in the Pa- (Charlson et al., 1987; Gage et al., 1997; De Clerck et al.,
laeoproterozoic, around 1.2 billion years ago, the engulfment 2018). The origin and diversification of green algae lays the
of a cyanobacterium by a heterotrophic unicellular foundations for the modern diversity of green plants, and this

© 2022 Institute of Botany, Chinese Academy of Sciences

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Journal of Integrative Plant Biology Evolutionary history of green plants

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-
Figure 1. The phylogeny, ecology and morphology of green algae
The phylogeny of the main lineages of green algae is a composite of widely diation and understanding of evolution of innovative traits.
accepted relationships based on molecular data (Leliaert et al., 2019; Del Here, we review recent progresses in the elucidation of
Cortona et al., 2020; Li et al., 2020, 2021a). Uncertain phylogenetic rela- origin and evolutionary scenarios of green plants, mainly fo-
tionships are indicated by polytomies. Different colors indicate the main
cusing on the three key evolutionary events. We discuss the
habitats of each lineage: blue‐marine; green‐freshwater; orange‐terrestrial.
The drawings show the main morphology of each lineage, and illustrate the phylogenetic affinities of green plants, propose a reliable
transformation from ancestral unicellularity to complex multicellularity in timescale for plant evolution, and summarize the adaptive
green algae. Ulvophyceae s.s. represents the Ulvophyceae lineage except mechanisms of green plants that enabled their adaptations
for Bryopsidales.
and diversifications. This review expands our knowledge of
the evolution of green plants and highlights key scientific is-
sues that require further investigations in plant evolution.
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 THE PHYLOGENETIC
second key evolutionary event in the history of green plants RELATIONSHIP AND TIMESCALE
(Figure 2). The colonization of the terrestrial realms by early OF EARLY GREEN PLANTS
land plants remarkably contributes to the increase of primary
productivity and new habitats for animals that increased their Complex phylogenetic affinities of green algae
diversity (Parnell and Foster, 2012; One Thousand Plant Early green plants initially diversified as unicellular plank-
Transcriptomes Initiative, 2019). Which specific lineage of tonic algae in the oceans, and gave rise to the Prasino-
streptophyte algae gave rise to land plants is the fundamental dermophyta and Chlorophyta. Unicellular green algae from
question in tracing the evolutionary history of land plants. early diverging lineages were referred to as prasinophytes,
Recent large‐scale phylogenomic studies based on plastid and approximately nine clades of the prasinophytes were
and nuclear genes supported that the Zygnematophyceae identified, forming a paraphyletic assemblage of scaled/
was the sister group to land plants, which had simple cyto‐ naked, flagellated/non‐flagellated microalgae (Leliaert et al.,
morphology (i.e., unicellular and filamentous) (Zhong et al., 2012; Lemieux et al., 2014; Fang et al., 2017; Leliaert et al.,
2013, 2014; One Thousand Plant Transcriptomes Initiative, 2019). Recent phylogenomic studies have greatly improved
2019). Interestingly, in higher‐branching streptophyte algae the relationships of prasinophytes. The Prasinococcales
(the Zygnematophyceae, Coleochaetophyceae and Char- (clade VI) together with the Palmophyllales (Palmophyllo-
ophyceae grade, the ZCC grade), Zygnematophyceae are phyceae) occupied the deepest branch of the prasinophytes
simple unicellular and filamentous forms, and Chara from (Leliaert et al., 2016). The Pyramimonadales (clade I)+Ma-
Charophyceae possess high degrees of organismal com- miellophyceae (clade II) formed the second‐deepest clade,
plexity, such as the stonewort with rhizoids and stem‐like and the more recently diverging groups included the
structures (Hori et al., 2014; Nishiyama et al., 2018; Cheng Nephroselmidophyceae (clade III), Pycnococcaceae (clade
et al., 2019; Liang et al., 2020). Thus, the origin of land plants V) and other lineages (clades VIIA and VIIC) (Lopes dos
is referred to as the evolutionary singularity, due to the Santos et al., 2017). Notably, the circumscription of the
enigmatic origin of various traits of land plants. prasinophytes has changed with the Prasinoderma coloniale
The flourishing of seed plants has shaped the terrestrial genome, which placed Palmophyllophyceae as the earliest‐
ecosystem, and angiosperms undoubtedly dominated recent branching green plants, unveiling the existence of a novel
ecological history on land. Angiosperms have surpassed phylum within green plants–the Prasinodermophyta (Figure 1;
gymnosperms to be the most diverse land plants, due to a Li et al., 2020). This finding underscores the need for generating
rapid radiation and diversification around 130 Ma (Figure 2). more genomic resources for early branching green algae, which
The rapid radiation and diversification of angiosperms is the will shed new light on the evolutionary routes of early green
third key evolutionary event, which has been referred to as plants.

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Evolutionary history of green plants Journal of Integrative Plant Biology

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).

Prasinophytes gave rise to the core Chlorophyta that in- topologies highly supported that Trebouxiophyceae, the
cludes unicellular and multicellular species, a major group of earliest diverging branch of UTC, was a monophyletic group,
green algae diversified in marine, freshwater and terrestrial comprising two different branches: Chlorellales and core
environments. The core Chlorophyta includes three large Trebouxiophyceae. Ulvophyceae has been resolved as pol-
classes (Ulvophyceae, Trebouxiophyceae and Chlor- yphyletic, including two monophyletic groups: Bryopsidales
ophyceae: UTC) and two small classes (Pedinophyceae and and remaining Ulvophyceae (hereafter Ulvophyceae s.s.)
Chlorodendrophyceae) (Figure 1). The monophyletic group of (Fang et al., 2018; Del Cortona et al., 2020; Li et al., 2021a).
Chlorophyceae have been widely supported by both molec- Pedinophyceae and Chlorodendrophyceae were the early‐
ular and ultrastructural data (Mattox and Stewart, 1984; diverging groups of the core Chlorophyta, while their
Lemieux et al., 2015; Fučíková et al., 2016; Sun et al., branching order remained in conflict (Fang et al., 2018; Li
2016; Fang et al., 2018). In terms of Trebouxiophyceae, re- et al., 2021a).
cent nuclear phylogenomic analyses yielded phylogenetic Reconstructing an accurate phylogeny of anciently di-
trees that were congruent with that from chloroplast ge- verged lineages of green plants presents a serious challenge,
nomes (Del Cortona et al., 2020; Li et al., 2021a). These tree mainly due to the poor taxon sampling, molecular rate

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Journal of Integrative Plant Biology Evolutionary history of green plants

heterogeneity, and limitation of phylogenetic resolution pro- marked an increase in the level of complexity of green plants.
vided by current phylogenetic methods (Leliaert et al., Multicellularity has adaptive significance for green plants as it
2011, 2016). The phylogenetic incongruence among the five has enabled adaptation to complex and changeable envi-
major classes within the core Chlorophyta are subject to the ronments, as well as laying the foundation for the differ-
rate variation across lineages and amino acid/nucleotide entiation of tissues and organs in land plants (Umen, 2014).
compositional variation (Liu et al., 2014). The homogeneous
models could not fully consider the rate variation and com- The origin of early green plants and “Snowball Earth”
positional heterogeneity and instead exacerbate model mis- A reliable timescale of green plants provides a crucial
specification issues, which considerably reduce the phylo- framework for understanding plant taxonomy, ecological di-
genetic accuracy of green algae (Kapli et al., 2020). Fang versity and interactions and co‐evolution with the global cli-
et al. (2018) found that the main conflicts in chloroplast mate and various plant‐feeding organisms. Fossil records are
phylogeny of core Chlorophyta likely stem from the sub- direct evidence in dating the divergence time of early green
stantial GC‐heterogeneous sites. The phylogenetic inference plants. However, the algal fossils are largely acritarchs, and
of core Chlorophyta was greatly improved by progressively their scarcity, fragmentation and uncertainty in taxonomic
removing the most GC‐heterogeneous sites and applying affinities have largely hindered the accurate inference of the
heterogeneous models. Moreover, it is worth noting that origin time of green plants. For instance, Russian acritarchs
large‐scale datasets dramatically reduced stochastic errors (~2,000−1,800 Ma) are taxonomically ambiguous, which
in phylogenetic inference, but they simultaneously amplified might be representatives of either Chlorophyta or Strepto-
systematic errors when using inadequate models. Li et al. phyta, or even a common ancestor of these two groups. This
(2021a) emphasized the importance of an optimal com- acritarchs only assume that the common ancestor of Vir-
promise between genome‐scale data and various models, idiplantae and Rhodophyta have lived at least 2,000 Ma
and increased the supports of several controversial nodes (Teyssèdre, 2007). Although the recently discovered well‐
within and among the classes of core Chlorophyta. Although preserved fossils (Proterocladus antiquus) indicate that early
the taxon sampling in green algae has been recently ex- green plants, at least, have originated before 1,000 Ma, the
panded, the sampling of clades with notable ecological and precise taxonomic affinities of Proterocladus remained con-
morphological importance was still sparse. Future studies tentious (attributed to stem of Cladophorales or Ulvophy-
with intensive taxon sampling and better‐fitting evolutionary ceae) (Tang et al., 2020).
models, will greatly improve the resolution of the phyloge- The surge in molecular data of green algae, the opti-
netic relationship of green algae. mization of the molecular clock model and improvements in
fossil calibration methods offer great potential for investigating
Ecological and morphological diversification of early the origin time of green plants. Even with the improvements in
green plants models and methods, considerable disparities have been
Prasinophytes, the early diverging clades of the Chlorophyta, observed among the estimates of the divergence time of early
predominantly flourishes in marine environments. The green plants (ranging from Paleoproterozoic to Neo-
Chlorophyceae and Trebouxiophyceae mainly thrive in proterozoic) (Heckman, 2001; Hedges et al., 2004; Zimmer
freshwater and terrestrial environments, and most algae from et al., 2007; Herron et al., 2009; Blank, 2013; Leliaert et al.,
Ulvophyceae have benthic marine habitats (Figure 1; Becker 2016; Morris et al., 2018). For instance, Blank (2013) employed
and Marin, 2009; Leliaert et al., 2012). Based on the widely penalized likelihood and Bayesian methods, and inferred that
accepted phylogeny of Chlorophyta, it is reasonable to hy- green plants originated at Paleoproterozoic (1,900−1,520 Ma).
pothesize that early green algae originated from marine en- Morris et al. (2018) applied the independent‐rates (IR) model
vironments, and later independently adapted to freshwater using large‐scale nuclear data and showed that green plants
and terrestrial environments (Li et al., 2021a). The transition occurred at Neoproterozoic (972−670 Ma). Recently, Nie et al.
of habitats has shaped the cyto‐morphology diversification, (2020) took into account various sources of uncertainty,
likely by driving the evolution of mechanisms underlying the such as different calibration strategies, clock‐partitioning
cell division. For instance, both Ulvophyceae and prasino- schemes, tree topology and evolutionary rate heterogeneity,
phytes shared a similar type of microtubules‐mediated cy- and collectively inferred that the early green plants
tokinesis and marine habitat, and the secondary loss of originated in the Paleoproterozoic to Mesoproterozoi (1,679.7
phycoplast in Ulvophyceae likely resulted from the switch −1,025.6 Ma).
back to marine habitats from freshwater habitats (Lewis and Interestingly, this origin time of early green plants is ap-
McCourt, 2004; Del Cortona et al., 2020; Li et al., 2021a). It is propriately earlier than the massive glaciation events
worth noting that the early branching green algae were al- (“Snowball Earth”) in the Neoproterozoic era (Pierrehumbert
most unicellular, and multicellularity evolved independently in et al., 2011; Becker, 2013; Rooney et al., 2014; Prave et al.,
different clades of green algae (Cocquyt et al., 2010; Del 2016). The “Snowball Earth” hypotheses mainly have posited
Cortona et al., 2020; Li et al., 2021a). The transition from geological explanations for Neoproterozoic glaciation
unicellular to differentiated multicellular organisms was one (Hoffman and Schrag, 2002; Goddéris et al., 2003; Rooney
of the most important innovations in plant evolution, and it et al., 2014). Nie et al. (2020) investigated the roles and

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Evolutionary history of green plants Journal of Integrative Plant Biology

mechanisms of green algae in shaping the global climate and sampling of hornworts and eliminating the effect of syn-
emphasized their potential impacts on the formation of gla- onymous substitutions.
ciers. Overall, the timeline of early green plants has laid the Reconstructing an accurate phylogeny of early land plants
groundwork for gaining further insights into the evolutionary attracts considerable interest in investigating the evolution of
scenarios of green plants, as well as the history of global morphological and developmental characters, especially the
climates and ecosystems. 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-
STREPTOPHYTE ALGAE AND THE phyceae diverged after Chlorokybophyceae and Meso-
ORIGIN OF LAND PLANTS stigmatophyceae, and evolved multicellularity, forming
packets of cells or simple filaments (Becker and Marin,
The phylogeny and morphological evolution of early 2009; Leliaert et al., 2016). The algae in higher‐branching
land plants ZCC clade arising from the KCM clade at about 700 Ma, were
Much of our understanding of green plant evolution comes from the first green plants to house more than one plastid per cell
morphological and molecular evidence. However, the conflicts of (de Vries et al., 2016). Given that Zygnematophyceae are
evolutionary trajectory inferred from molecular and morpho- recognized as the closest algal relatives to the ancestors of
logical data still exist in green plants, especially in streptophyte land plants, their organismal complexity and lifestyles should
algae and early land plants. The surge in genomic data has have high similarities with the early land plants. Surprisingly,
greatly alleviated the sparse gene and taxon sampling in recent Zygnematophyceae have the least complex bodyplan of all
phylogenetic studies, and the branching order of streptophyte higher‐branching streptophyte algae, and they mainly are
algae and early land plants have been robustly resolved (Figure 2; unicellular and filamentous (Buschmann and Zachgo,
Puttick et al., 2018; de Sousa et al., 2019; One Thousand Plant 2016; Leliaert et al., 2019). It is worth mentioning that land
Transcriptomes Initiative, 2019; Su et al., 2021). The streptophyte plants have inherited their genetic materials from the ances-
algae were paraphyletic and comprised the basal‐branching tral green algae, whereas their complex organs and tissues,
Klebsormidiophyceae, Chlorokybophyceae, and Mesostig- appears to have evolved on land. For example, comparative
matophyceae (KCM) clade and the higher‐branching Zygnema- genomic analyses of two early‐diverging subaerial/terrestrial
tophyceae, Coleochaetophyceae, and Charophyceae (ZCC) Zygnematophyceae revealed that many genes essential for
clade. The notion, Zygnematophyceae representing the most embryophytes are present in the common ancestor of Zyg-
likely sister group of land plants, was strengthened by multiple nematophyceae and embryophytes (Cheng et al., 2019).
phylogenomic analyses (Zhong et al., 2013, 2014; Cheng et al., Nevertheless, various crucial traits (e.g., cuticle with stomata,
2019; One Thousand Plant Transcriptomes Initiative, 2019). trilete spores and a basic body organization comprising
Bryophytes (liverworts, mosses and hornworts) were the stems and reproductive structures) are unique features of
second‐most diverse group of land plants, and the rela- land plants (Gensel, 2008; Clarke et al., 2011).
tionships between bryophytes and tracheophytes have The question is not only what the first land plants looked
been vigorously debated. Early cladistic studies using like, but it is more interesting to figure out what contributes to
morphological and biochemical characters, as well as the shape these features. It is well documented that the shift from
mitochondrial multigene data, strongly supported the par- a haplobiontic life cycle with a single multicellular haploid
aphyly hypothesis of bryophytes (Mishler and Churchill, gametophytic generation (streptophyte algae) to a dip-
1985; Qiu et al., 2006; Qiu, 2008). The availability of large‐ lobiontic life cycle (land plants), characterized by an alter-
scale nuclear genes and application of more complex nation of multicellular haploid and diploid generations, oc-
evolutionary models have shown that bryophytes formed curred within green plants (Figure 2; Bowman et al.,
a monophyletic group, sister to the vascular plants 2016; Kenrick, 2017). Accordingly, it has been proposed that
(Figure 2; Puttick et al., 2018; de Sousa et al., 2019; Su the transition to land entailed changes in life cycle, and the
et al., 2021; Donoghue et al., 2021). The inconsistent re- accompanied substantial somatic development resulted in
lationships within bryophytes phylogeny is likely caused by the evolution of tissues and organs basic to land plants, in-
lineage‐specific differences of rate variation and deviating cluding stems, leaves, roots, a vascular system, stomata, and
amino acid/nucleotide composition. The widely accepted sex organs. Comparative analyses among chlorophyte algae
notion that bryophyte is a monophyletic group was pro- and land plants have pointed to the conservative evolutionary
posed and strengthened by a series of phylogenomic history of the TALE‐class homeobox genes involved in reg-
studies. Puttick et al. (2018) proposed the hypotheses that ulating haploid‐to‐diploid transition in green plants (Bowman
bryophytes were monophyletic, and de Sousa et al. (2019) et al., 2016; Horst et al., 2016). Variable gene expression has
further increased support for the monophyletic bryophytes been shown to help organisms to cope with multiple envi-
using the lineage‐heterogenous compositional model. Su ronmental stresses in the short term, and it might also trigger
et al. (2021) recently yielded highly supported mono- longer‐term adaptations during evolution by enhancing phe-
phyletic relationships of bryophytes by improving taxon notypic variability and robustness (López‐Maury et al., 2008).

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Journal of Integrative Plant Biology Evolutionary history of green plants

Thus, the shifting of expression patterns of TALE homeobox 2011; Hedges et al., 2018; Morris et al., 2018; Su et al.,
genes have been hypothesized to play important roles in 2021). Employing the maximum age of the oldest‐possible
transforming plant life cycles. The process that recruiting and non‐marine palynomorphs (515 Ma) as the maximum
integration of key traits evolved in distinct types of life cycles bound appeared to constrain the origin time of land plants
was also critical for the adaptations to land of green plants. within the narrow time interval, from Middle Cambrian to
For instance, stomata were thought to evolve in the spor- Early Ordovician (515−470 Ma) (Morris et al., 2018). This
ophytes with bryophyte‐like life cycles, facilitating spore strategy largely amplified the effects of maximum bound
dispersal (Kenrick, 2017). Stomata has been co‐opted with and ignored the contribution of molecular data in time es-
the gametophyte‐derived vasculature and rooting structures timation, resulting in a relative younger origin.
in the most recent common ancestor of vascular plants, Interestingly, when removing the maximum constraint,
laying the foundations of modern plant diversity (Duckett or using the more conservative time of 1 042 Ma (repre-
et al., 2009). senting a sampled Precambrian locality yielding no plant‐
It has been hypothesized that two consecutive bursts of like spores), the origin time of land plants have been es-
genomic novelty separately occurred in the ancestor of timated as much older (793−560 Ma (Hedges et al., 2018);
streptophytes and the ancestor of land plants, likely con- 815−568 Ma (Clarke et al., 2011)). Su et al. (2021) inves-
tributing to the origin of multicellularity and terrestrialization in tigated the impacts of different maximum bounds on
early land plants (Bowles et al., 2020). The bursts of genomic the origin of land plants and assumed a Precambrian
novelty likely resulted from possible whole genome duplica- (980−682 Ma) origin for land plants by considering the
tion (WGD) and horizontal gene transfer (HGT), which laid the reliability of fossil calibrations and the influence of mo-
foundations of vital biological functions, including phyto- lecular data. More importantly, Su et al. (2021) claimed
hormone signaling, cell wall and root development, and that fossil calibrations used to estimate the timescale of
gravitropism. The molecular and physiological mechanisms plant evolution need more scrutiny, and the important
underpinning the innovations of bodyplan of land plants re- contribution of molecular data (time‐dependent molecular
main largely elusive despite extensive investigations, and changes) should be valued when faced with controversial
more systematic studies are urgently needed. fossil evidence. Intriguingly, the recent discovery of a
fossil spore assemblage has documented an Early Ordo-
Timescale of land plants vician (480 Ma) origin of land plants, closing the gap be-
Concerns over divergence time estimates for land plants tween molecular and fossil estimates and supporting an
have attracted attentions of plant biologists and paleontolo- earlier origination of land plants (Strother and Foster,
gists, due to the time gap between molecular estimates and 2021). The high potential for fossil preservation of bryo-
fossil records. Macrofossils are typical land plants fossils, phyte material has raised the possibility of many exquisite
and those from early land plants are very sparse. At present, fossils of early land plants (Tomescu et al., 2018), which
the oldest macrofossil came from a primitive vascular plant, could provide novel information for exploring the timeline
Cooksonia cf. Pertoni, suggesting that land plants occurred of land plants and bring fossils and molecular estimates
at least in the Ludlow Silurian (426.9 Ma) (Edwards and into a closer alignment.
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 DARWIN'S “ABOMINABLE
permanent tetrads were regarded as spores of land plants MYSTERY” IN ANGIOSPERMAE
(Morris et al., 2018), and the well‐preserved cryptospores
(Tetrahedraletes cf. Medinensis) from the Dapingian Zanjon Complex evolutionary routes of angiosperms
Formation supported the origin time of land plants back to Angiosperms (flowering plants) are the most successful
469 Ma (Rubinstein et al., 2010). groups, exhibiting extensive morphological and ecological
Establishing a robust timescale requires using appro- diversity, and have great advantages in modern terrestrial
priate minimum and maximum constraints, and well‐dated ecosystems. The angiosperm phylogeny has been greatly
fossils only provide reliable minimum bounds. Maximum improved in the last two decades (Chase et al., 1993; Soltis
calibration is usually constrained in two ways: (i) assigning et al., 1999, 2011; Moore et al., 2007, 2010; Qiu et al.,
a parametric distribution on the age of the fossil (minimum) 2010; Ruhfel et al., 2014; Wickett et al., 2014; Zeng et al.,
calibration, such as the gamma, lognormal or the truncated 2014; Group et al., 2016; Zhong and Betancur‐R, 2017;
Gaussian distribution; (ii) assuming that a clade has not yet Gitzendanner et al., 2018; Givnish et al., 2018; One Thousand
evolved in a geologic period if there is an absence of fossils Plant Transcriptomes Initiative, 2019; Li et al., 2019). Most
in that period, in which case the upper bound of the period studies supported the Amborella‐sister hypothesis that Am-
is the maximum constraint for the clade. The maximum borella was the earliest diverging lineage of angiosperms,
constraint for crown land plants has been controversial, followed successively by Nymphaeales and Austrobaileyales
and different divergence times of land plants have been (Figure 2; Albert et al., 2013; Drew et al., 2014; Zhong and
obtained using various maximum bounds (Clarke et al., Betancur‐R, 2017; One Thousand Plant Transcriptomes

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Evolutionary history of green plants Journal of Integrative Plant Biology

Initiative, 2019; Zhang et al., 2020a). Particularly, early discordances in the backbone of angiosperm phylogeny
studies have questioned the basal position of Amborella, and (Guo et al., 2021; Ma et al., 2021).
regarded it as a phylogenetic artifact caused by long‐branch Due to the similar patterns of phylogenetic discordance pro-
attraction and poor fit between evolutionary models and se- duced by both processes, it appears to be difficult to exactly
quence data (Xi et al., 2014; Goremykin et al., 2013, 2015). distinguish hybridization from ILS. The relative contribution of ILS
Recent phylogenomic analyses with expanded taxon sam- or hybridization to phylogenetic conflicts also has not been
pling supported the Amborella‐sister hypothesis, by amelio- carefully evaluated. Assessing the relative influence of these two
rating potential systematic errors which arose from limited processes would greatly enhance our understanding of the
taxon sampling and gene tree estimation error (Zhong and evolutionary forces driving rapid radiation of angiosperms. More
Betancur‐R, 2017; One Thousand Plant Transcriptomes Ini- importantly, Yang et al. (2020a) uncovered that the polytomy
tiative, 2019; Li et al., 2021b). More attention should be paid among five major lineages of Mesangiospermae could not be
to alleviate the effects of poor fit between evolutionary rejected, implying that a strictly bifurcating tree might not ad-
models and sequence data, and explore the relative con- equately represent early radiation of angiosperms. Detecting the
tribution of biological factors (e.g., incomplete lineage sorting patterns of reticulation in the backbone of angiosperm phylogeny
(ILS), hybridization and gene duplication/loss) to phyloge- would allow for a more thorough understanding of the evolution
netic incongruence. of angiosperms.
The remaining angiosperms form a monophyletic clade,
Mesangiospermae, which is subdivided into five major The origin time of angiosperms and “Jurassic gap”
groups: eudicots, monocots, magnoliids, Chloranthales, and Compared with green algae and early land plants, the fossils
Ceratophyllales. Numerous phylogenomic studies using of seed plants are abundant and relatively reliable. As the
large‐scale nuclear genes supported monocots as sister to early branching seed plants, gymnosperms form a small
the rest of Mesangiospermae, whereas the branching order monophyletic group, comprising about 800 species (http://
of four remaining clades varied among different analyses www.mobot.org/MOBOT/research/APweb/), and gymno-
(Figure 2). One Thousand Plant Transcriptomes Initiative sperms and angiosperms have diverged in the Carboniferous
(2019) supported that eudicots+Ceratophyllales were sister (359−299 Ma) (Won and Renner, 2006). The first radiation of
to Magnoliids+Chloranthales, which has been recently con- angiosperms occurred in the early Cretaceous; however, few
firmed by genomic data (Guo et al., 2021; Ma et al., 2021). reliable fossil records of angiosperms have been found in
However, few studies have recovered alternative topologies strata prior to the Early Cretaceous (Herendeen et al., 2017).
among these clades (Zeng et al., 2014; Yang et al., 2020a). Although many older fossils have been reported, most of
For example, Zeng et al. (2014) reported that eudicots were them cannot stand up to scrutiny. For instance, Liaoning-
sister to Ceratophyllales+Chloranthales, which were in turn fructus ascidiatus, an early Cretaceous Yixian Formation
sister to Magnoliids. Meanwhile, the chloroplast phyloge- fossil found in Liaoning, was once thought to be an angio-
nomic analyses received topologies that magnoliids and sperm (Wang and Han, 2011). However, this fossil has now
Chloranthales were the successive sister to other Me- been reassessed as a conifer, as the initially interpreted
sangiospermae lineages (Li et al., 2019, 2021b), or the clade structure, the fruit with ascidiate carpels containing two
of Magnoliids and Chloranthales was sister to other Me- seeds is actually galls on the linear leaves of the conifer
sangiospermae lineages (Moore et al., 2007, 2010; Soltis (Liaoningocladus) (Wong et al., 2015). Similarly, fossils of
et al., 2011; Ruhfel et al., 2014; Gitzendanner et al., 2018). Euanthus panii and Aegianthus daohugensis from the Ju-
The discordance between nuclear and organellar phyloge- rassic have been carefully re‐examined, and the evidence for
nies has been widely observed at the deep levels of angio- them claimed as angiosperms was either weak or non-
sperm phylogeny, especially in the placement of monocots, existent (Krassilov and Bugdaeva, 1988, 1999; Zheng and
Magnoliids and Chloranthales (Soltis et al., 2011; Ruhfel Wang, 2010; Deng et al., 2014; Liu and Wang, 2016;
et al., 2014; Zeng et al., 2017; Gitzendanner et al., 2018; Herendeen et al., 2017). At present, the pollen fossils (espe-
Li et al., 2019; One Thousand Plant Transcriptomes cially the tricolpate pollen fossils) found in the Early Creta-
Initiative, 2019). ceous (~133–125 Ma) were widely accepted as angiosperm
Current studies mainly focused on dense taxon and gene fossil records (Barremian‐Aptian transition), which could be
sampling to reconstruct the angiosperm phylogeny, whereas reliably assigned as crown‐group angiosperms (Hughes and
few explicitly investigated the cause of phylogenetic conflicts McDougall, 1990; Hughes, 1994). However, most molecular
in the backbone of angiosperm phylogeny (Yang et al., clock studies indicated that angiosperms began to diverge
2020a, 2020b; Guo et al., 2021; Ma et al., 2021). The cyto- into modern groups at Jurassic or even earlier, suggesting
nuclear discordance and incongruence among nuclear gene the “Jurassic gap” between the fossil records and molecular
trees have been documented as the consequence of several clock estimates (Smith et al., 2010; Clarke et al., 2011; Zeng
evolutionary processes, including ILS, gene duplication and et al., 2014; Beaulieu et al., 2015; Barba‐Montoya et al.,
loss, and gene flow (hybridization and introgression). The 2018; Li et al., 2019; Yang et al., 2020a).
recent phylogenomic analyses have identified that both hy- In recent years, many studies have been devoted to
bridization and ILS together contributed to these explaining this temporal difference from various

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Journal of Integrative Plant Biology Evolutionary history of green plants

perspectives. Through a series of simulations, Beaulieu energy and signal source, due to the absorption of UV‐B and
et al. (2015) demonstrated that the potential biases red/far‐red light by water (Figure 3; Singh et al., 2015).
caused by rate heterogeneity between herbaceous and Cryptochrome is the well documented blue light photo-
woody species tended to generate the older age esti- receptor in plants, and it belongs to the cryptochrome/photo-
mates, especially large shifts in branch rates among early‐ lyases superfamily that highly diversified throughout the eukar-
diverging lineages of angiosperms. Recent studies have yotes (Losi and Gärtner, 2012; Fortunato et al., 2015). Both
revealed contrasting results, suggesting that rate hetero- cryptochrome and photolyases have the conserved DNA pho-
geneity had little effect on the age of crown angiosperms tolyase and flavin adenine dinucleotide (FAD) binding domains,
(Foster et al., 2017; Yang et al., 2020a). Given the im- whereas plant cryptochromes possess a cry carboxyterminal
portant contribution of phylogenetic information in Baye- extension (CCT), which is essential for mediating the light sig-
sian dating analyses, Brown and Smith (2018) highlighted naling (Liu et al., 2011, 2017; Zuo et al., 2011). Cryptochromes
that the configuration of statistical inference problems could absorb different light through the binding of chromo-
(e.g., parameters, relationships and associated priors) phores, including FAD for UV‐A and the light‐harvesting deaza-
might hinder the inference of the crown age of angio- flavin or pterin like 5,10‐methenyltetrahydrofolate (MTHF) for blue
sperms. Various molecular dating analyses all supported light (Falciatore and Bowler, 2005). In green plants, light could
a pre‐Cretaceous angiosperm origin by expanding taxon activate the nuclear‐localized cryptochromes to homodimerize
sampling and nuclear genes, and by considering the ef- and bind to downstream signaling components, regulating the
fects of different variables in the molecular clock (Barba‐ hypocotyl elongation, flowering and the circadian clock (Franklin
Montoya et al., 2018; Li et al., 2019; Yang et al., 2020a). et al., 2014; Christie et al., 2015).
The time gap between molecular data and fossil evidence Phototropins (PHOTs) are also the blue‐light receptors that
was a typical problem (Nel et al., 2013; Misof et al., 2014), originated in green plants. PHOTs control a series of photo-
and recent advances in palaeobotanical records have synthetic efficiency optimization in land plants, including photo-
narrowed the “Jurassic gap”. Shi et al. (2021) discovered tropism, light‐induced stomatal opening, and chloroplast move-
the early Cretaceous fossil assemblage in Inner Mongolia, ments in light intensity changing process (Christie, 2007). In the
and supported that the ancestral taxa of angiosperms model alga Chlamydomonas reinhardtii, photoactivated PHOT
emerged in the Triassic about 250 Ma, likely implying the could cause changes of expression levels of specific targets and
pre‐Cretaceous origin of angiosperms. Future discoveries was essential for its sexual life cycle completion and acclimation
of reliable fossils are needed to unravel the mysteries of to high‐light stress (Huang and Beck, 2003; Aihara et al., 2019).
the “Jurassic gap”. 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-
THE EVOLUTION OF LIGHT dicating that PHOTs originated within green plants (Li et al.,
2015a; Li and Mathews, 2016). Thus, it is reasonable to presume
SENSING AND SIGNALING IN
that the evolution of blue light signaling pathway provided the
GREEN PLANTS opportunity to sense and utilize the light in deep sea, facilitating
their survival and laying the foundations for subsequent terres-
What physiological properties allow the first land plants to
trialization.
thrive? Light is undoubtedly a predominant environmental
factor, and green plants have evolved complex light per-
ception and transduction pathways to immediately adjust UV RESISTANCE LOCUS 8 (UVR8): the sentinels of
UV‐B radiation in shallow water
their physiological responses, balancing the growth, devel-
During the transition from deep sea to shallow water, green algae
opments and stress response.
evolved the UV‐B signaling pathways, allowing them to survive
Cryptochromes and phototropins: Catching the first the high UV‐B irradiation in shallow water (Figure 3; Li and
flash of light in the deep sea Mathews, 2016; Aihara et al., 2019). High UV‐B irradiation con-
Light, one of the most influential environmental factors during stitutes a potential abiotic stress factor for photosynthetic plants
the life cycle of plants, not only fuels the plants through with sessile lifestyle, whereas low dose rates of UV‐B act as a
photosynthesis, but supplies critical cues of environments to signal to regulate plant photomorphogenesis and induce UV‐B
mediate their growth and developments, such as diurnal acclimation (Frohnmeyer and Staiger, 2003). UVR8 has been
rhythm and neighboring plants. The wavelength, intensity and characterized as the exclusive UV‐B photoreceptor in green
composition of light drastically change from deep sea to plants, and could sense UV‐B radiation via intrinsic tryptophan
water surface, from aquatic environment to dry land (Maberly, residues functioning as chromophores (Wu et al., 2012; Tilbrook
2014; Han et al., 2019). In response to corresponding light et al., 2016; Tossi et al., 2019). Phylogenetic studies indicated
signal variation, green plants have evolved different light that UVR8 is a specific UV‐B receptor and widely exists in most
sensory systems for light signal perception and transduction. clades of green plants (Fernández et al., 2016; Han et al., 2019).
From the origin of Archaeplastida, most ancient plants lived There have been two different types of UVR8‐mediated signaling
in the deep sea, and only utilized blue light as the main pathways: (1) the canonical UVR8‐COP1/SPA‐HY5‐RUP

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Evolutionary history of green plants Journal of Integrative Plant Biology

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 originate in
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.

signaling pathway; (2) the direct binding of UVR8 to specific types: (i) phyA is the only type I phytochrome (photo‐labile);
transcription factors (TFs) (Liang et al., 2018; Yang et al., (ii) phyB‐E are type II phytochromes (photo‐stable) (Quail,
2018, 2020c). Zhang et al. (2021) recently discovered that the 1997; Li et al., 2015b; Rockwell and Lagarias, 2020). Phyto-
canonical UVR8‐COP1/SPA‐HY5‐RUP signaling pathway origi- chromes generally occur in two reversible conformations: Pr
nated in chlorophytes, and the interactions between UVR8 and and Pfr, which could separately transit through red and far‐
downstream TFs mainly originated in charophytes and early land red light absorption, mediating the nucleus translocation and
plants. Moreover, the binding of UVR8 to specific TFs confers the contributing to the light responses and development (Franklin
cross‐talks between environmental UV‐B signal and hormonal and Quail, 2009; Strasser et al., 2010; Rausenberger et al.,
signal in green plants, likely expanding the repertoires of UV‐B 2011; Ádám et al., 2013; Hu et al., 2013; Klose et al.,
signaling pathway. Multiple UVR8‐mediated signaling pathways 2015; Sánchez‐Lamas et al., 2016). Plant phytochromes
ensure UV‐B signal transduction and physiological response, usually contain two modules, the photosensory module in N‐
reflecting the adaptations of green plants to the UV‐B radiation terminal of phytochromes including a Period/Arnt/Single‐
during terrestrialization. Minded (PAS) domain, a cGMP phosphodiesterase/adenylyl
cyclase/FhlA (GAF) domain, and a phytochrome‐specific
Phytochromes: the last step before slogging on land (PHY) domain; the output module in C‐terminal with two
During the adaptations to the subaerial/terrestrial habitats, tandem PAS domains termed PRD (PAS‐repeat domain) and
charophytes employ the phytochrome signaling pathway for a histidine kinase‐related domain (HKRD) (Krall and Reed,
acquiring red/far‐red light (600–750 nm) as the main energy 2000; Nagatani, 2010).
source and crucial light signal (Figure 3). Plant phytochromes In the past years, the origin and evolution of the phyto-
(encoded by PHYA‐PHYE) have been classified into two chrome signaling pathway have been well‐studied. Canonical

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Journal of Integrative Plant Biology Evolutionary history of green plants

phytochromes (plant phytochromes) have been widely iden- 2009; Jeong et al., 2010). Although the sequence and func-
tified in streptophytes, confirming the charophyte origin of tion of COP1 is highly conserved in plants and animals, SPA
the canonical phytochrome (Li et al., 2015b; Li and Mathews, and COP1/SPA complex formation are plant specific. COP1
2016). In contrast, the non‐canonical phytochrome com- and SPA have shown significant codivergence and strong
prised various types, and widely existed in glaucophytes, coevolution signals in angiosperms (Han et al., 2019). The
chlorophytes, fungi and bacteria (Rockwell and Lagarias, expansion of COP1 and SPA gene families in angiosperms
2020). Rather than origination through endosymbiotic gene might have promoted the formation of various COP1/SPA
transfer (EGT), several studies supported that multiple HGT complexes for response to different light conditions on land
events gave rise to extant eukaryotic phytochromes (Li et al., (Laubinger et al., 2004; Han et al., 2019; Xu et al., 2021).
2015b). Importantly, the fusion among phytochrome and Although cryptochromes and COP1 already existed in the
other different photoreceptors is a vital mechanism, driving ancestor of plants, the co‐evolution and optimization of light
its adaptation and evolution. Dualchrome1 (DUC1) and neo- perception and downstream signal transduction components
chromes were discovered as chimeric photoreceptors. evidently contributed to the plant terrestrialization. The
DUC1, consisting of a two‐domain fusion of PHY and CRY, UVR8‐mediated signaling pathways enabled plants to deal
originated from a prasinophyte alga, Pycnococcus provasolii with UV‐B in shallow water, and the phytochrome signaling
(Makita et al., 2021). Neochromes were fused by PHY and pathway helped plants to colonize the subaerial/terrestrial
PHOT, which were mostly discovered in ferns (Nozue et al., habitats. Acclimation to different distributions of light quality
1998; Kawai et al., 2003; Suetsugu et al., 2005). The photo- in new environments resulted in the origination and evolution
receptor chimera provides more efficient utilization of light in of specific light signaling pathways, ultimately contributing to
ferns and algae, and these discoveries raise interesting the complex light signaling networks in green plants.
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‐ THE INNOVATIONS OF GENETIC
tune the light regulatory networks for complicated terrestrial
VARIATION IN GREEN PLANTS
environments (Rensing, 2018).
The extent and role of HGT in the evolution of green
COP1‐SPA: The heart of light signaling networks plants
COP1 forms an E3 ubiquitin ligase complex together with the The process of genetic movement between species is re-
four SPAs (SPA1‐4), and COP1‐SPA complex directs ferred to as horizontal or lateral gene transfer (HGT or LGT).
photomorphogenesis‐promoting factors to be degraded HGT has long been regarded as a crucial evolutionary force
through the 26S proteasome system, resulting in the re- that drives the adaptations and diversities of prokaryotes
pression of photomorphogenesis in the dark (Lian et al., (Peter et al., 2002; Soucy et al., 2015), whereas more atten-
2011; Liu et al., 2011; Zuo et al., 2011; Lu et al., 2015; Sheerin tion has been devoted to investigating the HGT events from
et al., 2015; Balcerowicz et al., 2017; Podolec et al., 2021). bacteria/fungi to green plants with the increasing of genomic
Both COP1 and SPAs have the highly similar domains, in- data. The well‐known HGT event was the endosymbiotic
cluding a middle coiled‐coil domain and C‐terminal WD40 gene transfer of cyanobacterial genes into the eukaryotic
repeats, whereas COP1 possesses an additional N‐terminal host nuclear genome (Timmis et al., 2004), resulting in the
kinase‐like domain (Deng and Quail, 1992; Deng and Matsui, ancient photosynthetic eukaryotes. The acquisition of pho-
Wei, et al., 1992; Stoop‐Myer et al., 1999; Holm et al., tosynthetic ability from the acquired plastid had far‐reaching
2001; Menon et al., 2016). Photoactivated photoreceptors consequences for plant evolution, not only relieving the het-
could interact with the WD40 domain of COP1 via their VP erotrophic host from the dependency on the continuous up-
domains (cryptochromes and UVR8, sometimes phosphory- take of organic carbon, but conferring them the assimilating
lated), repressing its E3 ligase activity and releasing its sub- and metabolic functions of some organic/inorganic elements
strates for downstream signaling transduction (Osterlund (Weber and Flügge, 2002; Balk and Lobréaux, 2005; Wang
et al., 2000a, 2000b; Lau and Deng, 2012; Lau et al., 2019). It and Benning, 2012).
has been reported that COP1 originated in the common an- The acquisitions of novel genes through HGT in green
cestor of all eukaryotes (Han et al., 2020), whereas SPAs plants have been widely documented, and these HGT‐
were plant‐specific proteins, originating in chlorophytes derived genes are involved in various biological process,
(Figure 3; Xu et al., 2021). These studies indicated that the including DNA damage repair, starch metabolism, plant
interactions between SPAs and COP1 originated at least in defense and environmental stress response (Figure 4; Yue
early land plants, and SPAs likely experienced sub- et al., 2012; Soucy et al., 2015; Hirooka et al., 2017; Zhang
functionalization/neofunctionalization after its divergence in et al., 2020b). Especially, it has been shown that many HGT
the ancestor of euphyllophytes (ferns and seed plants) (Xu events occurred in charophytes and bryophytes, due to the
et al., 2021). COP1/SPA complexes serve as the central re- spatial proximity between them and soil bacteria/fungi,
pressor in multiple light signaling pathways, and activated likely facilitating the generation of innovative traits related
photoreceptors can repress their functions (Kang et al., to terrestrialization. For example, the common ancestor of

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Evolutionary history of green plants Journal of Integrative Plant Biology

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).

Zygnematophyceae and embryophytes have presumably regulators of plant growth and development (Cheng et al.,
acquired the PYR/PYL/RCAR and GRAS gene families from 2019). The transaldolase (TAL)‐type gene has been identi-
the soil bacteria through HGT, and they could separately fied as an HGT‐derived gene in the ancestor of strepto-
encode abscisic acid (ABA) receptors and essential phytes from bacteria, and transgenic experiments showed

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Journal of Integrative Plant Biology Evolutionary history of green plants

that knock‐down of TAL in rice could result in smaller and (One Thousand Plant Transcriptomes Initiative, 2019). Among
immature vascular bundles, implying the vital role of TAL in other plant lineages, 31% of the speciation events in ferns
plant vascular system development (Yang et al., were reported to be associated with genome duplication
2015b; Chen et al., 2021). (Wood et al., 2009), and three ancient WGDs were identified
It is no doubt that HGTs have occurred in some lineages along the phylogenetic backbone of ferns (Huang et al.,
of green plants, but the extent and role of HGTs in the evo- 2020). Recent studies have revealed that the mosses Syn-
lution of green plants appear to be overstated for various trichia caninervis and Physcomitrella patens shared an an-
reasons. The plant genomic data has shown great advan- cient WGD, and multiple ancient large‐scale duplication
tages in identifying HGT‐derived genes, whereas it also has events occurred in the ancestor of the bryophytes (Devos
amplified the potential false positives. The HGT‐derived et al., 2016; Gao et al., 2020; Silva et al., 2021). Compared to
genes in green plants were identified based on a combina- the extensive WGD in land plants, the evidence of WGD was
tion of sequence similarity searching and phylogenetic tree exclusively found in the early diverging Zygnematophyceae
reconstruction. This method is proved to be effective in (Spirogloea muscicola) (Cheng et al., 2019).
identifying HGT events among distantly related species (such Although many polyploidy events have been documented
as between bacteria/fungi and green plants), but we should throughout plant evolution, our knowledge about their evo-
be cautious to apply this to closely related species. Multiple lutionary consequences and impacts on plant ecology are
processes (e.g., introgression, gene duplication/loss and ILS) limited. Previous studies have shown that numerous WGDs
of gene evolution might produce similar tree topology, thus were not randomly distributed over time, but rather correlated
misleading us in assessing the extent of HGTs in green with periods of extinction or dramatic global change (Levin
plants. Another important factor of possible false positivity and Soltis, 2018; Wu et al., 2020; Koenen et al., 2021; Silva
was from genome contamination. Although the genome se- et al., 2021; Van de Peer et al., 2021). Multiple independent
quencing, assembly, and annotation approaches have been WGDs occurred around the Cretaceous‐Paleocene (K‐Pg)
greatly developed, the contaminations in plant genomes were boundary, implying the possible roles of WGDs in con-
still a non‐negligible issue due to the complex living con- tributing to the survival of species during the extinction event
ditions and lifestyles of plants. (Vanneste et al., 2014; Wu et al., 2020). Recent evidence has
It has been shown that the transferred genes were nearly indicated that gene families that contribute to adaptations to
neutral or at least harmless for the recipients (Gogarten and specific environmental changes were co‐retained duplicates
Townsend, 2005; Soucy et al., 2015). The HGT‐derived genes from a wave of independent polyploidy events, such as
might be recruited and experienced natural selection during global cooling and darkness during the K‐Pg boundary (Wu
evolution, resulting in the stable inheritance or loss of the et al., 2020). This study also demonstrated that different
transferred genes (Soucy et al., 2015). It was an exemplar families of TFs showed certain preferences of retention, and
case that plants evolved the capacity to produce toxins for key members in stress‐related networks commonly pre-
defense, and plant‐feeding insects acquire corresponding sented as high‐retention after multiple independent WGDs.
genes for detoxification through HGTs, representing a typical Analyses of ancient gene duplications in mosses have sug-
example of “arms race” driven by HGTs (Li et al., 2011; Xia gested that recurrent significant retention of stress‐related
et al., 2021). Nevertheless, the biological function of most genes might have contributed to their adaptations to distinct
identified HGT‐derived genes in green plants were largely ecological environments (Gao et al., 2020). Moreover, Soltis
unknown, which has limited the investigation of their sig- et al. (2015) have proposed that WGD might lead to a ge-
nificance in plant adaptation and evolution. Future work nomic combination for the origin of evolutionary novelty, re-
should strive to improve the methods for identifying HGT, sulting in a burst of diversification of green plants. Indeed,
investigate the mechanisms underpinning HGT, and explore many WGDs in green plants were proved to facilitate the
the evidences that evaluate the significance of HGT events. increase of species diversification rates. For example, Huang
et al. (2020) demonstrated that three WGDs along the back-
Extensive WGDs in land plants bone of fern phylogeny were positively correlated with their
Whole‐genome duplication, or polyploidy, has long been diversification rate shifts. Landis et al. (2018) revealed that 61
recognized as a ubiquitous phenomenon during land plant of 106 WGD events were associated with shifts in diversifi-
evolution. Numerous studies have implicated that recent and cation rates across angiosperm phylogeny, and these WGD
ancient polyploidization events occurred repeatedly events appeared to occur within a period of environmental
throughout all the major land plant lineages, with the most instability.
frequency of WGD in angiosperms (Figure 4; Jiao et al., Ancient WGDs were crucial driving forces that shaped
2011, 2014; Li et al., 2015c; Ren et al., 2018; One Thousand the origin of key innovations during plant evolution, es-
Plant Transcriptomes Initiative, 2019; Huang et al., 2020; Wu pecially in angiosperms. The ancient WGDs which oc-
et al., 2020; Zhang et al., 2020c; Stull et al., 2021). Ancient curred in early evolution of angiosperms were likely to be
polyploidy in the ancestry of angiosperms and seed plants responsible for several structural innovations of flowers,
has been identified (Jiao et al., 2011), and over 180 WGDs and most notable innovations were the developments of
have been further reported in all extant angiosperm lineages sealed carpel and true vessel elements in stem tissue

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Evolutionary history of green plants Journal of Integrative Plant Biology

(Carlquist and Schneider, 2002; Soltis et al., 2009; Soltis ACKNOWLEDGEMENTS

and Soltis, 2016). Another example was the rapid di-
versification of glucosinolate compounds in the Brassi- We greatly appreciate Hongzhi Kong for valuable comments,
cales. It has been demonstrated that most genes in the and three anonymous reviewers’ critical reading that helped
glucosinolate pathway were derived from WGDs in the improve the manuscript. We sincerely apologize to re-
history of Cleomaceae and Brassicaceae (Bergh et al., searchers whose studies were not included in this review
2016). The diversification of glucosinolate compounds owing to space constraints. This work is supported by the
that was facilitated by neofunctionalization of these du- National Natural Science Foundation of China (32122010,
plicate genes have contributed to the “arms race” be- 31970229 and 32100178), the Collaborative Innovation
tween plants and herbivores, influencing the terrestrial Center for Modern Crop Production co‐sponsored by Prov-
ecosystems (Edger et al., 2015). The understanding of ince and Ministry, and the Priority Academic Program De-
connections and mechanisms among WGDs, radiation, velopment of Jiangsu Higher Education Institutions (PAPD).
origin of innovative traits and adaptations still needed
future studies to advance our understanding of them. CONFLICTS OF INTEREST
The authors declare they have no conflicts of interest asso-
CONCLUSIONS AND ciated with this work.
PERSPECTIVES
In the past two decades, the phylogenetic resolution of AUTHOR CONTRIBUTIONS
green plants has been greatly improved with the growing
B.Z. conceived the project and designed the review; Z.Z., X.
wealth of genomic data from increasingly diverse sets of
M., Y.L., L.Y., X.S., H.W., and R.D. wrote the manuscript. All
species. However, there are several important aspects that
authors reviewed and approved of the manuscript.
we need to consider in future studies, such as the poor fit
between evolutionary models and molecular data, identi- Edited by: Zhizhong Gong, China Agricultural University, China
fying and assessing the biological factors in phylogenetic
inference, and the “time gap” between molecular estimates Received Oct. 23, 2021; Accepted Jan. 8, 2022; Published Jan. 12, 2022
and fossil records. Evolutionary biologists have been de-
FA: Free Access
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
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