Search

SUMMARY: The moss Physcomitrium patens is crucial for studying plant development and evolution. Although the P. patens genome includes genes acquired from bacteria, fungi and viruses, the functions and evolutionary significance of these acquired genes remain largely unclear. Killer protein 4 (KP4) is a toxin secreted by the phytopathogenic fungus Ustilago maydis that inhibits the growth of sensitive target strains by blocking their calcium uptake. Here, we show that KP4 genes in mosses were acquired from fungi through at least three independent events of horizontal gene transfer. Two paralogous copies of KP4 (PpKP4‐1 and PpKP4‐2) exist in P. patens. Knockout mutants ppkp4‐1 and ppkp4‐2 showed cell death at the protonemal stage, and ppkp4‐2 also exhibited defects in tip growth. We provide experimental evidence indicating that PpKP4‐1/2 affects P. patens protonemal cell development by mediating cytoplasmic calcium and that KP4 genes are functionally conserved between P. patens and fungi. The present study provides additional insights into the role of horizontal gene transfer in land plant development and evolution. Significance Statement: Plants are intimately associated with fungi. However, it remains largely unclear how fungi may have affected the biology of plant partners through genetic integration (e.g. horizontal gene transfer) following organismal interaction. In the present study, we show that KP4 genes in mosses were acquired from fungi through at least three independent horizontal gene transfer events and that the acquired KP4 genes affect the protonemal development of mosses. [ABSTRACT FROM AUTHOR]

How horizontal gene transfer (HGT) has contributed to the evolution of animals and plants remains a major puzzle. Despite recent progress, defining the overall scale and pattern of HGT events in land plants has been largely elusive. In this study, we performed systematic analyses for acquired genes in different plant groups and throughout land plant evolution. We found that relatively recent HGT events occurred in charophytes and all major land plant groups, but their frequency declined rapidly in seed plants. Two major episodes of HGT events occurred in land plant evolution, corresponding to the early evolution of streptophytes and the origin of land plants, respectively. Importantly, a vast majority of the genes acquired in the two episodes have been retained in descendant groups, affecting numerous activities and processes of land plants. We analyzed some of the acquired genes involved in stress responses, ion and metabolite transport, growth and development, and specialized metabolism, and further assessed the cumulative effects of HGT in land plants. The role of horizontal gene transfer in the evolution of multicellular eukaryotes such as plants and animals has long been elusive. This study identifies two major episodes of horizontal gene transfer in the evolution of land plants. Genes acquired from environmental organisms have fundamentally shaped the structure, physiology, and development of land plants. [ABSTRACT FROM AUTHOR]

Plant colonization of land has been intimately associated with mycorrhizae or mycorrhizae-like fungi. Despite the pivotal role of fungi in plant adaptation, it remains unclear whether and how gene acquisition following fungal interaction might have affected the development of land plants. Here we report a macro2 domain gene in bryophytes that is likely derived from Mucoromycota, a group that includes some mycorrhizae-like fungi found in the earliest land plants. Experimental and transcriptomic evidence suggests that this macro2 domain gene in the moss Physcomitrella patens, PpMACRO2, is important in epigenetic modification, stem cell function, cell reprogramming and other processes. Gene knockout and over-expression of PpMACRO2 significantly change the number and size of gametophores. These findings provide insights into the role of fungal association and the ancestral gene repertoire in the early evolution of land plants. Plant evolution is intimately associated with fungal partners. Here the authors provide evidence that Physcomitrella patens MACRO2, a gene likely derived from early mycorrhizae-like fungi, was transferred to early land plants and plays an important role in regulating stem cell growth and gametophore development in moss. [ABSTRACT FROM AUTHOR]

Cytokinin oxidase/dehydrogenase (CKX) is a key enzyme responsible for the degradation of endogenous cytokinins. However, the origins and roles of CKX genes in angiosperm evolution remain unclear. Based on comprehensive bioinformatic and transgenic plant analyses, we demonstrate that the CKXs of land plants most likely originated from an ancient chlamydial endosymbiont during primary endosymbiosis. We refer to the CKXs retaining evolutionarily ancient characteristics as "ancient CKXs" and those that have expanded and functionally diverged in angiosperms as "non-ancient CKXs". We show that the expression of some non-ancient CKXs is rapidly inducible within 15 min upon the dehydration of Arabidopsis, while the ancient CKX (AtCKX7) is not drought responsive. Tobacco plants overexpressing a non-ancient CKX display improved oxidative and drought tolerance and root growth. Previous mutant studies have shown that non-ancient CKXs regulate organ development, particularly that of flowers. Furthermore, ancient CKXs preferentially degrade cis-zeatin (cZ)-type cytokinins, while non-ancient CKXs preferentially target N6-(Δ2-isopentenyl) adenines (iPs) and trans-zeatins (tZs). Based on the results of this work, an accompanying study (Wang et al. 10.1038/s41438-019-0211-x) and previous studies, we hypothesize that non-ancient CKXs and their preferred substrates of iP/tZ-type cytokinins regulate angiosperm organ development and environmental stress responses, while ancient CKXs and their preferred substrates of cZs play a housekeeping role, which echoes the conclusions and hypothesis described in the accompanying report (Wang, X. et al. Evolution and roles of cytokinin genes in angiosperms 1: Doancient IPTs play housekeeping while non-ancient IPTs play regulatory roles? Hortic Res7, (2020). 10.1038/s41438-019-0211-x). [ABSTRACT FROM AUTHOR]

A major event in land plant evolution is the origin of vascular tissues, which ensure the long-distance transport of water, nutrients and organic compounds. However, the molecular basis for the origin and evolution of plant vascular tissues remains largely unknown., Here, we investigate the evolution of the land plant TAL-type transaldolase ( TAL) gene and its potential function in rice ( Oryza sativa) based on phylogenetic analyses and transgenic experiments, respectively., TAL genes are only present in land plants and bacteria. Phylogenetic analyses suggest that land plant TAL genes are derived from Actinobacteria through an ancient horizontal gene transfer (HGT) event. Further evidence reveals that land plant TAL genes have undergone positive selection and gained several introns following its acquisition by the most recent common ancestor of land plants. Transgenic plant experiments show that rice TAL is specifically expressed in vascular tissues and that knockdown of TAL expression leads to changes in both the number and pattern of vascular bundles., Our findings show that the ancient HGT of TAL from bacteria probably plays an important role in plant vascular development and adaptation to land environments. [ABSTRACT FROM AUTHOR]

Horizontal gene transfer (HGT) may not only create genome mosaicism, but also introduce evolutionary novelties to recipient organisms. HGT in plastid genomes, though relatively rare, still exists. HGT-derived genes are particularly common in unicellular photosynthetic eukaryotes and they also occur in multicellular plants. In particular, ancient HGT events occurring during the early evolution of primary photosynthetic eukaryotes were probably frequent. There is clear evidence that anciently acquired genes played an important role in the establishment of primary plastids and in the transition of plants from aquatic to terrestrial environments. Although algal genes have often been used to infer historical plastids in plastid-lacking eukaryotes, reliable approaches are needed to distinguish endosymbionts-derived genes from those independently acquired from preferential feeding or other activities. [ABSTRACT FROM AUTHOR]

Strigolactones (SLs) and karrikins (KARs) are butenolides that influence multiple aspects of plant growth and development. D14 and KAI2 are members of the α/β-fold hydrolase superfamily and act as receptors of SLs and KARs, as well as of unidentified endogenous KAI2-ligands (KLs). Phylogenetic analyses suggest that plant KAI2 was derived from bacterial RsbQ via horizontal gene transfer (HGT) before the emergence of streptophytes. The D14/KAI2 and RsbQ proteins share conserved tertiary structures and functional features. In this opinion article, we suggest that the acquisition of RsbQ by plant cells was fundamental to the formation of butenolide sensing systems. Recruitment of additional signal transduction components and gene duplication subsequently led to versatile butenolide signaling systems throughout land plants. Strigolactones (SLs) are not only phytohormones that play multiple roles in plant growth and development, but also rhizosphere signals for communication between plants and microbes. Karrikins (KARs) are exogenous compounds generated from burning vegetation which can stimulate seed germination. They contain a butenolide moiety similar to that of SLs. The KAR receptor KAI2 is believed to normally recognize endogenous karrikin-like compounds referred to as KAI2-ligands (KLs). The KAI2 signaling pathway influences various developmental and physiological processes in plants. The duplication and differentiation of KAI2 in seed plants led to the evolution of the SL receptor gene family D14. The perception and signaling of KLs by KAI2 is commonly considered to be a major innovation during the early evolution of land plants, but the origin of KAI2 and SL/KL signaling system is unclear. [ABSTRACT FROM AUTHOR]

Although it is known that novel genes facilitated plant colonization of land, the evolutionary origin of these genes remains largely unclear. A recent study by Cheng et al. suggests that some key genes related to plant development and stress responses were acquired from soil bacteria during the early evolution of land plants. [ABSTRACT FROM AUTHOR]

Stomata are distributed in nearly all major groups of land plants, with the only exception being liverworts. Instead of having stomata on sporophytes, many complex thalloid liverworts possess air pores in their gametophytes. At present, whether stomata in land plants are derived from a common origin remains under debate. 1,2,3 In Arabidopsis thaliana , a core regulatory module for stomatal development comprises members of the bHLH transcription factor (TF) family, including AtSPCH , AtMUTE , and AtFAMA of subfamily Ia and AtSCRM1/2 of subfamily IIIb. Specifically, AtSPCH, AtMUTE, and AtFAMA each successively form heterodimers with AtSCRM1/2, which in turn regulate the entry, division, and differentiation of stomatal lineages. 4,5,6,7 In the moss Physcomitrium patens , two SMF (SPCH , MUTE and FAMA) orthologs have been characterized, one of which is functionally conserved in regulating stomatal development. 8,9 We here provide experimental evidence that orthologous bHLH TFs in the liverwort Marchantia polymorpha affect air pore spacing as well as the development of the epidermis and gametangiophores. We found that the bHLH Ia and IIIb heterodimeric module is highly conserved in plants. Genetic complementation experiments showed that liverwort SCRM and SMF genes weakly restored a stomata phenotype in atscrm1 , atmute , and atfama mutant backgrounds in A. thaliana. In addition, homologs of stomatal development regulators FLP and MYB88 also exist in liverworts and weakly rescued the stomatal phenotype of atflp/myb88 double mutant. These results provide evidence not only for a common origin of all stomata in extant plants but also for relatively simple stomata in the ancestral plant. • No evidence exists for bHLH Ia gene duplication in the ancestral land plant • The bHLH Ia/IIIb regulatory module is highly conserved in land plants • MpSMF and MpSCRM1/2 affect the development of the epidermis and gametangiophores • MpSMF weakly complements the functions of AtMUTE and AtFAMA The bHLH Ia/IIIb regulatory module plays a key role in stomata development. Chang et al. suggest that bryophyte SMF transcription factors possess functions partially similar to AtMUTE and AtFAMA. The stomatal development in the ancestral land plant most likely involved bHLH Ia transcription factors similar to SMF in extant bryophytes. [ABSTRACT FROM AUTHOR]

Horizontal gene transfer (HGT) refers to the movement of genetic material between distinct species by means other than sexual reproduction. HGT has contributed tremendously to the genome plasticity and adaptive evolution of prokaryotes and certain unicellular eukaryotes. The evolution of green plants from chlorophyte algae to angiosperms and from water to land represents a process of adaptation to diverse environments, which has been facilitated by acquisition of genetic material from other organisms. In this article, we review the occurrence of HGT in major lineages of green plants, including chlorophyte and charophyte green algae, bryophytes, lycophytes, ferns, and seed plants. In addition, we discuss the significance of horizontally acquired genes in the adaptive innovations of green plants and their potential applications to crop breeding and improvement. • HGT is important for adaptive innovation and widespread in all major green plant lineages. • Green plants have acquired many genes related to stress responses. • The ancestor of green plants acquired some essential genes for the innovation of carbon and energy metabolism. • Some genes acquired by charophytes had further exapted into the functions that are important in plant terrestrialization. • Most HGT genes in non-seed plants are from bacteria, fungi or viruses, while plant-to-plant HGT is frequent in seed plants. [ABSTRACT FROM AUTHOR]