Fig 2 - uploaded by Jan de Vries
Content may be subject to copyright.
![The earliest land plants: an evolutionary scenario for the conquest of land by streptophytes. Streptophyte algae are the only photosynthetic
eukaryotes from which the macroscopic land flora evolved (red lines). That said, throughout the course of evolution, algae from various other lineages
have colonized land (yellow lines)—but also streptophyte algae have continuously and independently made the wet to dry transition (convergence
of red and yellow). Throughout history, numerous lineages have become extinct (‘x’ labels). Terrestrial algae of various taxonomic affiliations dwell on
rock surfaces and form biological soil crusts. From the diversity of the paraphyletic streptophyte algae, however, did an organism whose descendants
eventually conquered land on a global scale emerge: a likely branched filamentous—or even parenchymatous—organism that formed rhizoidal structures
and experienced desiccation from time to time. From this ‘hypothetical hydro-terrestrial alga’, the lineages of Zygnematophyceae and embryophytes
(land plants) arose. In its infancy, the trajectory leading to the embryophytes was represented by the—now extinct (see also Delaux et al., 2019)—earliest
land plants. The earliest land plants probably interacted with beneficial substrate microbiota that aided them in obtaining nutrients from their substrate.
Furthermore, the earliest land plants had to successfully overcome a barrage of terrestrial stressors (including UV and photosynthetically active irradiance,
drought, drastic temperature shifts, etc.). They succeeded because they had the right set of traits—a mix of adaptations that were selected for in their
hydro-terrestrial algal ancestors, exaptations, and the potential for co-option of a fortuitous set of genes and pathways. During the course of evolution,
some members of the populations of the earliest land plants gained traits that are adaptive in terrestrial environments (such as some form of water
conductance, stomata-like structures, embryos, etc.); eventually, the ‘hypothetical last common ancestor of land plants’ emerged. From this ancestor,
the extant bryophytes and tracheophytes evolved. While the exact trait repertoire of the hypothetical last common ancestor of land plants is uncertain, it
will certainly have entailed properties of vascular and non-vascular plants. What is also certain is that the last common ancestor of land plants had traits
of algal ancestry. (All dating is roughly based on Morris et al. [2018])](profile/Jan-De-Vries-3/publication/338539991/figure/fig3/AS:954983293939712@1604697168148/The-earliest-land-plants-an-evolutionary-scenario-for-the-conquest-of-land-by.png)
The earliest land plants: an evolutionary scenario for the conquest of land by streptophytes. Streptophyte algae are the only photosynthetic eukaryotes from which the macroscopic land flora evolved (red lines). That said, throughout the course of evolution, algae from various other lineages have colonized land (yellow lines)—but also streptophyte algae have continuously and independently made the wet to dry transition (convergence of red and yellow). Throughout history, numerous lineages have become extinct (‘x’ labels). Terrestrial algae of various taxonomic affiliations dwell on rock surfaces and form biological soil crusts. From the diversity of the paraphyletic streptophyte algae, however, did an organism whose descendants eventually conquered land on a global scale emerge: a likely branched filamentous—or even parenchymatous—organism that formed rhizoidal structures and experienced desiccation from time to time. From this ‘hypothetical hydro-terrestrial alga’, the lineages of Zygnematophyceae and embryophytes (land plants) arose. In its infancy, the trajectory leading to the embryophytes was represented by the—now extinct (see also Delaux et al., 2019)—earliest land plants. The earliest land plants probably interacted with beneficial substrate microbiota that aided them in obtaining nutrients from their substrate. Furthermore, the earliest land plants had to successfully overcome a barrage of terrestrial stressors (including UV and photosynthetically active irradiance, drought, drastic temperature shifts, etc.). They succeeded because they had the right set of traits—a mix of adaptations that were selected for in their hydro-terrestrial algal ancestors, exaptations, and the potential for co-option of a fortuitous set of genes and pathways. During the course of evolution, some members of the populations of the earliest land plants gained traits that are adaptive in terrestrial environments (such as some form of water conductance, stomata-like structures, embryos, etc.); eventually, the ‘hypothetical last common ancestor of land plants’ emerged. From this ancestor, the extant bryophytes and tracheophytes evolved. While the exact trait repertoire of the hypothetical last common ancestor of land plants is uncertain, it will certainly have entailed properties of vascular and non-vascular plants. What is also certain is that the last common ancestor of land plants had traits of algal ancestry. (All dating is roughly based on Morris et al. [2018])
Source publication
Embryophytes (land plants) can be found in almost any habitat on Earth's surface. All of this ecologically diverse embryophytic flora arose from algae through a singular evolutionary event. Traits that were, by their nature, indispensable for the singular conquest of land by plants were those that are key for overcoming terrestrial stressors. Not s...
Similar publications
Genus Rubus represents the second largest genus of the family Rosaceae in Taiwan, with 41 currently recognized species across three subgenera ( Chamaebatus , Idaoeobatus , and Malochobatus ). Despite previous morphological and cytological studies, little is known regarding the overall phylogenetic relationships among the Rubus species in Taiwan, an...
Polyploidization is a major driving force in plant evolution. Allopolyploidization, involving hybridization and genome doubling, can cause extensive transcriptome reprogramming which confers allopolyploids higher evolutionary potential than their diploid progenitors. To date, little is known about the interplay between hybridization and genome doub...
Seeds were a key evolutionary innovation. These durable structures provide a concerted solution to two challenges on land: dispersal and stress. Lipid droplets (LDs) that act as nutrient storage reservoirs are one of the main cell-biological reasons for seed endurance. Although LDs are key structures in spermatophytes and are especially abundant in...
Land plant evolution is a major leap in the history of life that took place during the Neoproterozoic Era (~800 Mya). Charophyceae, a class of rhyzophytic green algae emerged as a land plant with innovations in biochemical, cytological and developmental adaptations and played a crucial role in establishing life on the land. One such striking archit...
The E3 ubiquitin ligases have been known to intrigue many researchers to date, due to their heterogenicity and substrate mediation for ubiquitin transfer to the protein. HECT (Homologous to the E6-AP Carboxyl Terminus) E3 ligases are spatially and temporally regulated for substrate specificity, E2 ubiquitin-conjugating enzyme interaction, and chain...
Citations
... Last but not the least importantly, meristem cells gain the ability to divide three-dimensionally, thereby increasing the number of cell layers in their matlike body, called thallus, and the capability to form various cell types (Jill Harrison, 2017). In addition to these morphological modifications, early land plants also have installed a chemical defense system that enables them to deal with oxidative stress, which can result from various kinds of abiotic stress, which are almost inevitable in a terrestrial habitat (de Vries and Archibald, 2018;Furst-Jansen et al., 2020). To cope with oxidative stress, all land plants have developed a sophisticated system consisting of chemical antioxidants, enzymatic catalysts, and a chemical shield against UV light (Noctor et al., 2016). ...
To adapt to a terrestrial habitat, the ancestors of land plants must make several morphological and physiological modifications, such as a meristem allowing for three-dimensional growth, rhizoids for water and nutrient uptake, air pore complexes or stomata that permit air exchange, and a defense system to cope with oxidative stress that occurs frequently in a terrestrial habitat. To understand how meristem is determined during land plant evolution, we characterized the function of the closest PLETHORA homolog in the liverwort Marchantia polymorpha, which we named MpPLT. Through transgenic approach, we showed that MpPLT is expressed not only in the stem cells at the apical notch but also in the proliferation zone of the meristem, as well as cells that form the air-pore complex and rhizoids. Using the CRISPR method we then created mutants for MpPLT and found that the mutants are not only defective in meristem maintenance but also compromised in air-pore complex and rhizoid development. Strikingly, at later developmental stages, numerous gemma-like structures were formed in Mpplt mutants, suggesting developmental arrest. Further experiments indicate that MpPLT promotes plant growth by regulating MpWOX, which shared a similar expression pattern as MpPLT, and genes involved in auxin and cytokinin signaling pathways. Through transcriptome analyses, we found that MpPLT also has a role in redox homeostasis and that this role is essential to plant growth. Together, these results suggest that MpPLT has a crucial role in liverwort growth and development and hence may have played a crucial role in early land plant evolution.
... Today, this relationship is exemplified through plants exchanging a reliable carbon source via the products of photosynthesis (i.e., sugars and fatty acids) and nearly ubiquitous symbiosis with filamentous fungi that exchange nitrogen, phosphorous, micronutrients, metabolites, and water retention (Bonfante & Genre, 2010;Martin & Nehls, 2009). Further, modern plant and fungal symbionts have been shown to mitigate many shared stresses such as oxidative, osmotic, heat, UV radiation, and rapid temperature flux (de Vries & Archibald, 2018;Du et al., 2019;Fürst-Jansen et al., 2020;Jermy, 2011;Kohler et al., 2015;Lutzoni et al., 2018). These same stresses would have posed significant barriers to entry for the first terrestrial land plants as well. ...
The model moss species Physcomitrium patens has long been used for studying divergence of land plants spanning from bryophytes to angiosperms. In addition to its phylogenetic relationships, the limited number of differential tissues, and comparable morphology to the earliest embryophytes provide a system to represent basic plant architecture. Based on plant–fungal interactions today, it is hypothesized these kingdoms have a long‐standing relationship, predating plant terrestrialization. Mortierellaceae have origins diverging from other land fungi paralleling bryophyte divergence, are related to arbuscular mycorrhizal fungi but are free‐living, observed to interact with plants, and can be found in moss microbiomes globally. Due to their parallel origins, we assess here how two Mortierellaceae species, Linnemannia elongata and Benniella erionia , interact with P. patens in coculture. We also assess how Mollicute ‐related or Burkholderia ‐related endobacterial symbionts (MRE or BRE) of these fungi impact plant response. Coculture interactions are investigated through high‐throughput phenomics, microscopy, RNA‐sequencing, differential expression profiling, gene ontology enrichment, and comparisons among 99 other P. patens transcriptomic studies. Here we present new high‐throughput approaches for measuring P. patens growth, identify novel expression of over 800 genes that are not expressed on traditional agar media, identify subtle interactions between P. patens and Mortierellaceae, and observe changes to plant–fungal interactions dependent on whether MRE or BRE are present. Our study provides insights into how plants and fungal partners may have interacted based on their communications observed today as well as identifying L. elongata and B. erionia as modern fungal endophytes with P. patens .
... The conquest of land by plants is one of the most consequential events in the evolution of life. While there are few fossils of those early land plants, recent analyses place this event around 550 mya ago (Morris et al., 2018;Fürst-Jansen et al., 2020). However, even the first land plants were not alone in this new habitat. ...
... It is believed that the ability to form symbiotic relationships with some of those organisms already present was a prerequisite for the successful establishment of plant life on land (de Vries and Rensing, 2020). The presence of regulatory systems controlled by phytohormones is often considered another requirement for the landfall by plants (Wang et al., 2015;Fürst-Jansen et al., 2020). Phytohormones are small compounds that regulate various aspects of plant life, such as the interaction with abiotic and biotic environments and the control of developmental processes. ...
... It was generally assumed that if the respective genes are present in the respective genome, they would work in the same way as in Arabidopsis and rice. However, for several phytohormones, it has been shown that although the members of the signaling pathway are present, they function in different ways (Yasumura et al., 2007;Fürst-Jansen et al., 2020;Feng et al., 2023). This strongly highlights the need for experimental evidence to understand the evolution of a given pathway. ...
Introduction
Cytokinins, a group of adenine derivatives, are phytohormones that regulate many aspects of the plant's reaction to changes in the abiotic and biotic environment and ensure the correct execution of developmental programs. While the signaling pathway and its effects are very well established for Angiosperms, its origin, and evolution are less well understood.
Methods
The first step in the analysis of the cytokinin signaling pathway is to test if the organism can react to the hormone. Thus, an assay was established, that uses differences in the growth pattern of the Streptophyte alga, Coleochaete scutata , to determine if this algal species reacts to different cytokinins.
Results
Surprisingly not only classical cytokinins, such as trans -zeatin and kinetin, led to a change in the pattern of growth, but also adenine, which is usually used as a negative control.
Discussion
This raises questions about the origin and the functioning of the cytokinin signaling in C. scutata and also in algae in general.
... In fact, the genes used in land plants to cope with these stress factors, can be found in Streptophyte algae (Fürst-Jansen et al. 2020). Whether they are integrated in the same functional context, is not fully demonstrated, yet. ...
Stress resilience is central for plant survival. The appropriate adaptive response not only depends on the type of stress, but also on the context with other stresses, the developmental state of the plant, and the history of preceding stress experiences. The response to stress combinations cannot be a mere addition of the responses to the individual factors. For instance, heat stress requires stomatal opening to cool the leaf by increased transpiration, while drought stress needs stomatal closure to reduce water loss by transpiration. However, heat and drought are often coming in concert, such that the plant needs to reach a prioritised decision. Thus, the response to stress combinations constitutes a new quality transcending the addition of individual stress components. In other words: to survive under combined stress, plants need to render real decisions. We propose a model, where different stress inputs share one or more transducing elements, that can be recruited for different downstream pathways. Competition for these shared elements allows for such qualitative decisions, depending on the relative activities in upstream signalling of the individual stress components. Using different types of osmotic stress as paradigm I demonstrates, how signal modularity and differences in temporal sequence can generate qualitatively different outputs. Thus, plant-stress signalling makes use of a limited set of molecular players to generate, by specific rules for their combination and sequence, different “meanings”. This can be compared to human language, where information-bearing elements (words) are combined according to grammatical rules to generate a semantic space. (249 words)
... Charophyceae, along with the Zygnematophyceae and the Coleochaetophyceae, form the ZCC grade, from which the common ancestor of land plants evolved Hess et al., 2022;Wickett et al., 2014;Wodniok et al., 2011). While Zygnematophyceae are the sister group to, and share a last common ancestor with, land plants (Cheng et al., 2019;Ruhfel et al., 2014;Wickett et al., 2014), the earlier branching Charophyceae form the only class that includes streptophyte algae with tissue-like structures and functional rhizoids (Bonnot et al., 2019), traits that were probably already possessed by the common ancestor of land plants, at least in a rudimentary fashion (Fürst-Jansen et al., 2020). Moreover, Charophyceae of the ZCC grade possess a huge cellulose-pectin-based cell wall with many polymers similar to land plants as well as plasmodesmata (Mikkelsen et al., 2014;Sørensen et al., 2011;Umen, 2014), which are features relevant for the successful colonization of the terrestrial habitat. ...
Charophyceae are the most complex streptophyte algae, possessing tissue‐like structures, rhizoids and a cellulose‐pectin‐based cell wall akin to embryophytes. Together with the Zygnematophyceae and the Coleochaetophycae, the Charophyceae form a grade in which the Zygnematophyceae share a last common ancestor with land plants. The availability of genomic data, its short life cycle, and the ease of non‐sterile cultivation in the laboratory have made the species Chara braunii an emerging model system for streptophyte terrestrialization and early land plant evolution. In this study, tissue containing nodal cells was prepared under the stereomicroscope, and an RNA‐seq dataset was generated and compared to transcriptome data from whole plantlets. In both samples, transcript coverage was high for genes encoding ribosomal proteins and a homolog of the putative PAX3‐ and PAX7‐binding protein 1. Gene ontology was used to classify the putative functions of the differently expressed genes. In the nodal cell sample, main upregulated molecular functions were related to protein, nucleic acid, ATP‐ and DNA binding. Looking at specific genes, several signaling‐related genes and genes encoding sugar‐metabolizing enzymes were found to be expressed at a higher level in the nodal cell sample, while photosynthesis‐and chloroplast‐related genes were expressed at a comparatively lower level. We detected the transcription of 21 different genes encoding DUF4360‐containing cysteine‐rich proteins. The data contribute to the growing understanding of Charophyceae developmental biology by providing a first insight into the transcriptome composition of Chara nodal cells.
... Double-negative signaling ensures that resources are allocated strategically and minimally to maintain plant well-being and reproduction, even under challenging environmental conditions. Indeed, the emergence of new signaling innovations and new hormone modules in land plants can be attributed to their need to adapt to a more challenging environment characterized by drought, nutrient deficiency stresses, temperature fluctuations, increased UV-B exposure, and heightened oxidative stress, which is a combination of both increased number of ROS-generating stressors and the fact that, unlike algae, land plants cannot readily release reactive oxygen species (ROS) or ROS-generating compounds into their surroundings [23,[117][118][119]. The transition from aquatic to terrestrial habitats brought about significant changes not only in abiotic stress factors but also in the biotic stress environment for land plants. ...
Biological modularity refers to the organization of living systems into separate functional units that interact in different combinations to promote individual well-being and species survival. Modularity provides a framework for generating and selecting variations that can lead to adaptive evolution. While the exact mechanisms underlying the evolution of modularity are still being explored, it is believed that the pressure of conflicting demands on limited resources is a primary selection force. One prominent example of conflicting demands is the trade-off between survival and reproduction. In this review, we explore the available evidence regarding the modularity of plant hormones within the context of the survival-reproduction trade-off. Our findings reveal that the cytokinin module is dedicated to maximizing reproduction, while the remaining hormone modules function to ensure reproduction. The signaling mechanisms of these hormone modules reflect their roles in this survival-reproduction trade-off. While the cytokinin response pathway exhibits a sequence of activation events that aligns with the developmental robustness expected from a hormone focused on reproduction, the remaining hormone modules employ double-negative signaling mechanisms, which reflects the necessity to prevent the excessive allocation of resources to survival.
... The evolution of plants for land colonization triggered the production of a wide array of signaling molecules that modulate gene expression and protein activities associated with abiotic stress tolerance (Ishizaki, 2017). These molecular changes include genes involved in responding to reduced water availability and excessive light, encompassing signaling pathways related to antioxidant defenses and morphological adaptations (Fürst-Jansen et al., 2020). Many of these genes are conserved and can be found from lycophytes to flowering plants (Ishizaki, 2017). ...
... Many of these genes are conserved and can be found from lycophytes to flowering plants (Ishizaki, 2017). The emergence and diversification of these genes related to transcription factors and stress-induced proteins represent a significant milestone in the increase of plant diversity and facilitated colonization across a range of wet to dry terrestrial environments, as they trigger biochemical and structural adjustments that allowed the plants cope with stress conditions (Fürst-Jansen et al., 2020). ...
The Isoëtes genus comprises a basal lineage of vascular plants with a wide distribution, including aquatic and terrestrial species, which can be attributed to environmental changes throughout its evolutionary history. The underwater quillwort, Isöetes cangae, is endemic to Lake Amendoim in the northern Amazon rainforest region of Brazil. To aid conservation strategies, we investigated the molecular and physiological changes associated with water column reduction and tolerance to terrestrial environments. Remarkably, this aquatic species has demonstrated a tolerance for periods without a water column during ex situ cultivation. Short-term experimental conditions (24 h) revealed upregulation of stress-related genes, while biochemical, morphological, and physiological parameters remained unchanged. In contrast, long-term terrestrial conditions (3–6 months) induced changes in the physiology and morphology of I. cangae, including an increase in antioxidant capacity, photoprotective mechanisms, and the preservation of reproductive structures. The Crassulacean Acid Metabolism was present in both aquatic and terrestrial conditions. Mature and immature spores were able to produce plants even after 12 months of desiccation, with desiccated spores generating more progeny than submerged spores.
... Although the ROS wave was shown to primarily propagate through the vascular bundles of Arabidopsis in response to a local HL stress (37), in response to a local wounding or heat stress (HS) treatments, it could also propagate through nonvascular tissues (i.e., mesophyll cells; ref. 38). We therefore extended our study to include Bryophytes (hornworts, liverworts, and mosses) that emerged from an early split in the diversification of land plants and lack lignified vascular tissues (39). A localized treatment of HL caused the activation of a rapid systemic ROS signal in Anthoceros agrestis (a Hornwort), Marchantia polymorpha (a Liverwort), and Physcomitrium patens (a Moss), with an average velocity of 0.13 cm min −1 (Fig. 1A and SI Appendix, Fig. S2 and Table 1). ...
Cell-to-cell communication is fundamental to multicellular organisms and unicellular organisms living in a microbiome. It is thought to have evolved as a stress- or quorum-sensing mechanism in unicellular organisms. A unique cell-to-cell communication mechanism that uses reactive oxygen species (ROS) as a signal (termed the "ROS wave") was identified in flowering plants. This process is essential for systemic signaling and plant acclimation to stress and can spread from a small group of cells to the entire plant within minutes. Whether a similar signaling process is found in other organisms is however unknown. Here, we report that the ROS wave can be found in unicellular algae, amoeba, ferns, mosses, mammalian cells, and isolated hearts. We further show that this process can be triggered in unicellular and multicellular organisms by a local stress or H2O2 treatment and blocked by the application of catalase or NADPH oxidase inhibitors and that in unicellular algae it communicates important stress-response signals between cells. Taken together, our findings suggest that an active process of cell-to-cell ROS signaling, like the ROS wave, evolved before unicellular and multicellular organisms diverged. This mechanism could have communicated an environmental stress signal between cells and coordinated the acclimation response of many different cells living in a community. The finding of a signaling process, like the ROS wave, in mammalian cells further contributes to our understanding of different diseases and could impact the development of drugs that target for example cancer or heart disease.
... The PAL-dependent pathway is less-explored as a source for SA in land plants compared to ICS-dependent synthesis of SA. The PALdependent pathway, despite being highly radiated, has homologs for all enzymes being present at least in the last common ancestor of all streptophytes-going hand in hand with the idea that parts of this pathway were part of the genetic building blocks that allowed for the radiation of specialized metabolism in land plants (Dadras et al., 2023;Fürst-Jansen et al., 2020). This is most likely explained by the fact that this pathway is not a highly specialized pathway for SA biosynthesis, but instead recruits steps from other pathways, such as the phenylpropanoid pathway. ...
Despite its small size, the water fern Azolla is a giant among plant symbioses. Within each of its leaflets, a specialized leaf cavity is home to a population of nitrogen-fixing cyanobacteria (cyanobionts). Although a number of plant-cyanobiont symbioses exist, Azolla is unique in that its symbiosis is perpetual: the cyanobionts are inherited during sexual and vegetative propagation. What underpins the communication between the two partners? In angiosperms, the phytohormone salicylic acid (SA) is a well-known regulator of plant-microbe interactions. Using high-performance liquid chromatography-tandem mass spectrometry, we pinpoint the presence of SA in the fern. Comparative genomics and phylogenetics on SA biosynthesis genes across Chloroplastida reveal that the entire Phenylalanine ammonia-lyase-dependent pathway likely existed in the last common ancestor of land plants. Indeed, Azolla filiculoides secondarily lost its isochorismate synthase but has the genetic competence to derive SA from benzoic acid; the presence of SA in artificially cyanobiont-free Azolla supports the existence of this route. Global gene expression data and SA levels from cyanobiont-containing and -free A. filiculoides link SA synthesis with the symbioses: SA appears to induce cyanobacterial proliferation, whereas removal of the symbiont results in reduced SA levels in a nitrogen-dependent manner.
... AAOs and TYRs might be responsible for the oxidation and polymerization of the phenolic products in these species. A small number of genes associated with the phenylpropanoid biosynthesis were also found in the nonstreptophyte and streptophyte algae we analysed, agreeing with the notion that the phenylpropanoid biosynthetic genes were present in streptophyte algae [35] [36], and even in chlorophytes [5,[36][37][38]. ...
... AAOs and TYRs might be responsible for the oxidation and polymerization of the phenolic products in these species. A small number of genes associated with the phenylpropanoid biosynthesis were also found in the nonstreptophyte and streptophyte algae we analysed, agreeing with the notion that the phenylpropanoid biosynthetic genes were present in streptophyte algae [35] [36], and even in chlorophytes [5,[36][37][38]. ...
... Dotted lines mean the species-dependent retention of COs among the species. Note: As there were aquatic, semi-terrestrial, and terrestrial species in the groups of chlorophytes, streptophyte algae, bryophytes, ferns, and seed plants [36], this figure represents only the habitats of the exampled species. ...
Phenolics are vital for the adaptation of plants to terrestrial habitats and for species diversity. Phenoloxidases (catechol oxidases, COs, and laccases, LACs) are responsible for the oxidation and polymerization of phenolics. However, their origin, evolution, and differential roles during plant development and land colonization are unclear. We performed the phylogeny, domain, amino acids, compositional biases, and intron analyses to clarify the origin and evolution of COs and LACs, and analyzed the structure, selective pressure, and chloroplast targeting to understand the species-dependent distribution of COs. We found that Streptophyta COs were not homologous to the Chlorophyta tyrosinases (TYRs), and might have been acquired by horizontal gene transfer from bacteria. COs expanded in bryophytes. Structural-functionality and selective pressure were partially responsible for the species-dependent retention of COs in embryophytes. LACs emerged in Zygnemaphyceae, having evolved from ascorbate oxidases (AAOs), and prevailed in the vascular plants and strongly expanded in seed plants. COs and LACs coevolved with the phenolic metabolism pathway genes. These results suggested that TYRs and AAOs were the first-stage phenoloxidases in Chlorophyta. COs might be the second key for the early land colonization. LACs were the third one (dominating in the vascular plants) and might be advantageous for diversified phenol substrates and the erect growth of plants. This work provided new insights into how phenoloxidases were evolved and devoted to plant evolution.
