Rhizospheric microbiomics integrated with plant transcriptomics provides insight into the Cd response mechanisms of the newly identified Cd accumulator Dahlia pinnata

Abstract

Phytoremediation that depends on excellent plant resources and effective enhancing measures is important for remediating heavy metal-contaminated soils. This study investigated the cadmium (Cd) tolerance and accumulation characteristics of Dahlia pinnata Cav. to evaluate its Cd phytoremediation potential. Testing in soils spiked with 5-45 mg kg^-1 Cd showed that D. pinnata has a strong Cd tolerance capacity and appreciable shoot Cd bioconcentration factors (0.80-1.32) and translocation factors (0.81-1.59), indicating that D. pinnata can be defined as a Cd accumulator. In the rhizosphere, Cd stress (45 mg kg^-1 Cd) did not change the soil physicochemical properties but influenced the bacterial community composition compared to control conditions. Notably, the increased abundance of the bacterial phylum Patescibacteria and the dominance of several Cd-tolerant plant growth-promoting rhizobacteria (e.g., Sphingomonas, Gemmatimonas, Bryobacter, Flavisolibacter, Nocardioides, and Bradyrhizobium) likely facilitated Cd tolerance and accumulation in D. pinnata. Comparative transcriptomic analysis showed that Cd significantly induced (P < 0.001) the expression of genes involved in lignin synthesis in D. pinnata roots and leaves, which are likely to fix Cd²⁺ to the cell wall and inhibit Cd entry into the cytoplasm. Moreover, Cd induced a sophisticated signal transduction network that initiated detoxification processes in roots as well as ethylene synthesis from methionine metabolism to regulate Cd responses in leaves. This study suggests that D. pinnata can be potentially used for phytoextraction and improves our understanding of Cd-response mechanisms in plants from rhizospheric and molecular perspectives.

Keywords: Dahlia pinnata; heavy metal contamination; phytoextraction; rhizobacteria; signal transduction.

Figure 1

Cd tolerance and accumulation characteristics of Dahlia pinnata. (A) Greenhouse pot experiments growing D pinnata in soils spiked with 0 (Cd0), 5 (Cd5), 20 (Cd20), and 45 mg kg^–1 Cd (Cd45). Biomass yields (B), Cd concentrations (C), bioconcentration factors (D), translocation factors (E), and Cd content (F) in D. pinnata under different treatments. Data represent means ± standard deviations (B–F: n = 3). Bars of the same color labeled with different letters indicate significant differences (P < 0.05, analysis of variance and Tukey’s test) between groups. DW: dry weight.

Figure 2

Rhizospheric bacterial community composition of Dahlia pinnata grown in soils spiked with 0 (Cd0) and 45 mg kg^–1 Cd (Cd45). (A) Principal component analysis (PCA) of operational taxonomic units (OTUs). Venn diagram of bacterial OTUs (B), phyla (C), and genera (D) between Cd0 and Cd45 soils. Relative abundance of bacterial phyla (E) and genera (F) that differ between Cd0 and Cd45 soils. P < 0.05, significant using Welch’s t-test.

Figure 3

Transcriptomic analysis and qRT‐PCR validation for Dahlia pinnata grown in control and Cd treatment (50 mM, 48 h) conditions. (A) Morphology of D. pinnata after experimental treatment under hydroponic conditions. (B) Principal component analysis (PCA) based on unigene abundance. (C) Volcano plot of differentially expressed genes (DEGs) between control and Cd-treated roots. (D) Volcano plot of DEGs between control and Cd-treated leaves. (E) Venn diagram showing DEG variation between roots and leaves. (F) Linear regression of gene expression changes between RNA sequencing and qRT‐PCR for 10 selected genes in roots and leaves. RCt, control group of root; RCd, Cd-treated group of root; LCt, control group of leaf; LCd, Cd-treated group of leaf.

Figure 4

Enriched KEGG pathways (P < 0.001) of up-regulated genes in roots (A) and leaves (B) of Dahlia pinnata grown in control and Cd treatment (50 mM, 48 h) conditions.

Figure 5

Schematic of Cd response processes of Dahlia pinnata grown in control and Cd treatment (50 mM, 48 h) conditions. Specific processes in roots and leaves are represented using red and blue arrows, respectively; common processes are represented using black arrows. ABA, abscisic acid; CaM/CML, calmodulin/calmodulin-like; CDPK, calcium-dependent protein kinase; ETH, ethylene; MAPK, mitogen-activated protein kinase; MAPKK, MAPK kinase; MAPKKK, MAPKK kinase; NO, nitric oxide; NOS, NO synthase.