Genome mining reveals abiotic stress resistance genes in plant genomes acquired from microbes via HGT

Abstract

Colonization by beneficial microbes can enhance plant tolerance to abiotic stresses. However, there are still many unknown fields regarding the beneficial plant-microbe interactions. In this study, we have assessed the amount or impact of horizontal gene transfer (HGT)-derived genes in plants that have potentials to confer abiotic stress resistance. We have identified a total of 235 gene entries in fourteen high-quality plant genomes belonging to phyla Chlorophyta and Streptophyta that confer resistance against a wide range of abiotic pressures acquired from microbes through independent HGTs. These genes encode proteins contributed to toxic metal resistance (e.g., ChrA, CopA, CorA), osmotic and drought stress resistance (e.g., Na⁺/proline symporter, potassium/proton antiporter), acid resistance (e.g., PcxA, ArcA, YhdG), heat and cold stress resistance (e.g., DnaJ, Hsp20, CspA), oxidative stress resistance (e.g., GST, PoxA, glutaredoxin), DNA damage resistance (e.g., Rad25, Rad51, UvrD), and organic pollutant resistance (e.g., CytP450, laccase, CbbY). Phylogenetic analyses have supported the HGT inferences as the plant lineages are all clustering closely with distant microbial lineages. Deep-learning-based protein structure prediction and analyses, in combination with expression assessment based on codon adaption index (CAI) further corroborated the functionality and expressivity of the HGT genes in plant genomes. A case-study applying fold comparison and molecular dynamics (MD) of the HGT-driven CytP450 gave a more detailed illustration on the resemblance and evolutionary linkage between the plant recipient and microbial donor sequences. Together, the microbe-originated HGT genes identified in plant genomes and their participation in abiotic pressures resistance indicate a more profound impact of HGT on the adaptive evolution of plants.

Keywords: abiotic stress resistance; horizontal gene transfer; microbe; phylogeny; plant.

Figure 1

Phylogenetic tree of metal resistance proteins in plant genomes originated from microbial taxa. The phylogeny construction was conducted based on gene-translating protein sequences using PhyML program with the Maximum Likelihood (ML) method and 1,000 bootstrap replicates (with bootstrap values in red showing on respective branches). Branches leading to plant taxa are marked by green color, whereas those belonging to microbial lineages are in black: (A) chromate transporters (ChrA); (B) copper homeostasis protein (CutC); (C) magnesium and cobalt transport protein (CorA). (D) phosphatase.

Figure 2

Phylogenetic tree of osmotic and drought stress resistance proteins in plant genomes originated from microbial taxa. The phylogeny construction was conducted based on gene-translating protein sequences using PhyML program with the Maximum Likelihood (ML) method and 1,000 bootstrap replicates (with bootstrap values in red showing on respective branches). Branches leading to plant taxa are marked by green color, whereas those belonging to microbial lineages are in black. (A) sodium/proton antiporter (CPA1); (B) Na⁺/solute symporter; (C) chloride channel protein (ClcA); (D) dTDP-D-glucose 4,6-dehydratase (RmlB).

Figure 3

Phylogenetic tree of heat and cold stress as well as oxidative stress resistance proteins in plant genomes originated from microbial taxa. The phylogeny construction was conducted based on gene-translating protein sequences using PhyML program with the Maximum Likelihood (ML) method and 1,000 bootstrap replicates (with bootstrap values in red showing on respective branches). Branches leading to plant taxa are marked by green color, whereas those belonging to microbial lineages are in black: (A) heat-shock protein DnaJ; (B) heat shock protein Hsp20; (C) cold-shock protein CspA; (D) peroxiredoxin; (E) heme peroxidase (PoxA); (F) glutathione S-transferase (GST).

Figure 4

Phylogenetic tree of acid resistance and DNA damage resistance proteins in plant genomes originated from microbial taxa. The phylogeny construction was conducted based on gene-translating protein sequences using PhyML program with the Maximum Likelihood (ML) method and 1,000 bootstrap replicates (with bootstrap values in red showing on respective branches). Branches leading to plant taxa are marked by green color, whereas those belonging to microbial lineages are in black. (A) arginine deiminase (ArcA); (B) basic amino acid/polyamine antiporter (YhdG); (C) chloride channel protein (ClcA); (D) dTDP-D-glucose 4,6-dehydratase (RmlB).

Figure 5

A case-study of microbe-originated plant cytochrome P450 and its donor protein. (A) Phylogenetic tree of the organic pollutant catabolism protein cytochrome P450 constructed by PhyML program with the Maximum Likelihood (ML) method and 1,000 bootstrap replicates (with bootstrap values shown by size of symbols); (B) structure perdition (deep-learning-driven) and comparison of representative recipient plant cytochrome P450 (left, Chlamydomonas reinhardtii: XP_001698815) and its putative microbial donor (right, Synechocystis sp. PCC: WP_028946589); (C) ligand-protein simulation diagram (5 ns classical molecular dynamics) of cytochrome P450 from Chlamydomonas reinhardtii (XP_001698815) showing key residues in proteins interacting with the hame prothetic group (ligand). Interactions that occur more than 30.0% of the simulation time in the selected trajectory (0.0 through 5.0 ns), are shown; (D) ligand-protein simulation diagram (5 ns classical molecular dynamics) of the cytochrome P450 from donor Synechocystis sp. PCC (WP_028946589) showing key residues in proteins interacting with the hame prothetic group (ligand) for comparison.

Figure 6

Ranges of codon adaption index (CAI) values of different kinds of abiotic resistance genes with EF-Tu gene as a reference.