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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]

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]

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]