Major episodes of horizontal gene transfer drove the evolution of land plants

Ma, Jianchao; Wang, Shuanghua; Zhu, Xiaojing; Sun, Guiling; Chang, Guanjun; Li, Linhong; Hu, Xiangyang; Zhang, Shouzhou; Zhou, Yun; Song, Chun‐Peng; Huang, Jinling

doi:10.1016/j.molp.2022.02.001

Cited by 78 publications

(76 citation statements)

References 95 publications

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“…A recent study identified two major episodes of HGT events during the evolution of streptophytes, corresponding to the early evolution of streptophyte algae and the origin of embryophytes, respectively. 64 Phylogenomics indicates the common ancestor of Zygnematophyceae and embryophytes acquired a LPR1-type MCO from soil bacteria during the first episode, corroborating previous notions that overcoming the challenges of plant terrestrialization profoundly benefited from HGT events. 52 , 55 Although a function of LPR1 in root Pi sensing has been established in Arabidopsis , 15 , 16 , 18 , 20 , 21 , 31 which is likely conserved in the tracheophyte lineage (vascular plants) as recently reported for rice, 46 , 47 the biological role of LPR1-like ferroxidases for Pi nutrition in the bryophyte lineage (nonvascular plants) and in extant Zygnematophyceae algae remains an open question.…”

Section: Discussionsupporting

confidence: 81%

“… 55 Our study supports the recent conjecture that multiple HGT events from soil bacteria to streptophyte progenitors accelerated plant terrestrialization. 50 , 55 , 63 , 64 For example, gene orthologs of two protein families that enforce land plant resilience, the GIBBERELLIC ACID INSENSITIVE [GAI]/REPRESSOR OF GAI/SCARECROW (GRAS) transcription factors and PYRABACTIN RESISTANCE1 [PYR1]/PYR1-LIKE/REGULATORY COMPONENTS OF ABSCISIC ACID RECEPTORS (PYR/PYL/RCAR)-like abscisic acid receptors, are present in soil bacteria and Zygnomatophyceae algae. Phylogenetic analyses of both gene families indicate HGT from soil bacteria followed by diversification in the embryophytes.…”

Section: Discussionmentioning

confidence: 99%

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Bacterial-type ferroxidase tunes iron-dependent phosphate sensing during Arabidopsis root development

et al. 2022

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Section: Discussionsupporting

confidence: 81%

Section: Discussionmentioning

confidence: 99%

Bacterial-type ferroxidase tunes iron-dependent phosphate sensing during Arabidopsis root development

et al. 2022

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“…Genome analysis of subaerial Zygnematophyceae algae concluded that gene families that increase resistance to biotic and abiotic stresses in land plants, in particular desiccation through abscisic acid (ABA), were acquired by HGT from soil bacteria (47). A recent work analyzed HGT patterns in 12 representative plant species (48). The authors identified two major HGT episodes in plant evolution, each of which contributed more than 100 gene families.…”

Section: Discussionmentioning

confidence: 99%

Widespread horizontal gene transfer between plants and their microbiota

Haimlich

Fridman

Khandal

et al. 2022

Preprint

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Plants host a large array of commensal bacteria that interact with the host. The growth of both bacteria and plants is often dependent on nutrients derived from the cognate partners, and the bacteria fine-tune host immunity against pathogens. This ancient interaction is common in all studied land plants and is critical for proper plant health and development. We hypothesized that the spatial vicinity and the long-term relationships between plants and their microbiota may promote or even depend on cross-kingdom horizontal gene transfer (HGT), a phenomenon that is relatively rare in nature. To test this hypothesis we analyzed the Arabidopsis thaliana genome and its extensively sequenced microbiome to detect events of horizontal transfer of full length genes that are absent from non-plant associated bacteria. Interestingly, we detected 180 unique genes that were horizontally transferred between plants and their microbiota. Genes transferred from plants to their microbiota are enriched in secreted proteins that metabolize carbohydrates, whereas microbes transferred to plants genes that are enriched in redox homeostasis functions. To validate our approach, we tested if a bacterial gene is functionally similar to its Arabidopsis homologue in planta. The Arabidopsis DET2 gene is essential for biosynthesis of the brassinosteroid phytohormones and loss-of-function of the gene leads to dwarfism. We found that expression of the DET2 homologue from Leifsonia bacteria of the Actinobacteria phylum in the Arabidopsis det2 background complements the mutant, and leads to normal plant growth. Together, these data suggest that cross-kingdom horizontal gene transfer events shape the interactions between plants and their microbiome.

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“…Many of these genes are involved in essential or plant-specific activities, such as xylem formation, plant defense, nitrogen recycling, and the biosynthesis of starch, polyamines, hormones, and glutathione. Clearly, HGT has played an important role in the direction and the rate of evolution in plants (Ma et al, 2022).…”

Section: Punctuated Evolution Driven By Horizontal Gene Transfermentioning

confidence: 99%

Rapid acquisition of microorganisms and microbial genes can help explain punctuated evolution

Rosenberg

2022

Front. Ecol. Evol.

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The punctuated mode of evolution posits that evolution occurs in rare bursts of rapid evolutionary change followed by long periods of genetic stability (stasis). The accepted cause for the rapid changes in punctuated evolution is special ecological circumstances – selection forces brought about by changes in the environment. This article presents a complementary explanation for punctuated evolution by the rapid formation of genetic variants in animals and plants by the acquisition of microorganisms from the environment into microbiomes and microbial genes into host genomes by horizontal gene transfer. Several examples of major evolutionary events driven by microorganisms are discussed, including the formation of the first eukaryotic cell, the ability of some animals to digest cellulose and other plant cell-wall complex polysaccharides, dynamics of root system architecture, and the formation of placental mammals. These changes by cooperation were quantum leaps in the evolutionary development of complex bilolgical systems and can contribute to an understanding of the mechanisms underlying punctuated evolution.

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Major episodes of horizontal gene transfer drove the evolution of land plants

Cited by 78 publications

References 95 publications

Bacterial-type ferroxidase tunes iron-dependent phosphate sensing during Arabidopsis root development

Bacterial-type ferroxidase tunes iron-dependent phosphate sensing during Arabidopsis root development

Widespread horizontal gene transfer between plants and their microbiota

Rapid acquisition of microorganisms and microbial genes can help explain punctuated evolution

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