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. 2022 Mar 2:13:841366.
doi: 10.3389/fpls.2022.841366. eCollection 2022.

Ethylene Response Factor109 Attunes Immunity, Photosynthesis, and Iron Homeostasis in Arabidopsis Leaves

Chiu-Ling Yang  1 , Yu-Ting Huang  1 , Wolfgang Schmidt  2 , Patricia Klein  3 , Ming-Tsair Chan  4 , I-Chun Pan  1
Affiliations

Ethylene Response Factor109 Attunes Immunity, Photosynthesis, and Iron Homeostasis in Arabidopsis Leaves

Chiu-Ling Yang et al. Front Plant Sci. .

Abstract

Iron (Fe) is an essential micronutrient element for all organisms including plants. Chlorosis of young leaves is a common symptom of Fe deficiency, reducing the efficiency of photosynthesis, and, ultimately, crop yield. Previous research revealed strong responsiveness of the putative key transcription factor ERF109 to the Fe regime. To elucidate the possible role of ERF109 in leaf Fe homeostasis and photosynthesis, we subjected Arabidopsis thaliana erf109 knockout lines and Col-0 wild-type plants to transcriptome profiling via RNA-seq. The transcriptome profile of Fe-sufficient erf109 leaves showed a 71% overlap with Fe-deficient Col-0 plants. On the other hand, genes that were differentially expressed between Fe-deficient and Fe-sufficient Col-0 plants remained unchanged in erf109 plants under conditions of Fe deficiency. Mutations in ERF109 increased the expression of the clade Ib bHLH proteins bHLH38, bHLH39, bHLH101, the nicotianamine synthase NAS4, and the Fe storage gene FER1. Moreover, mutations in ERF109 led to significant down-regulation of defense genes, including CML37, WRKY40, ERF13, and EXO70B2. Leaves of erf109 exhibited increased Fe levels under both Fe-sufficient and Fe-deficient conditions. Reduced Fv/Fm and Soil Plant Analysis Development (SPAD) values in erf109 lines under Fe deficiency indicate curtailed ability of photosynthesis relative to the wild-type. Our findings suggest that ERF109 is a negative regulator of the leaf response to Fe deficiency. It further appears that the function of ERF109 in the Fe response is critical for regulating pathogen defense and photosynthetic efficiency. Taken together, our study reveals a novel function of ERF109 and provides a systematic perspective on the intertwining of the immunity regulatory network and cellular Fe homeostasis.

Keywords: ERF109; RRTF1; immunity; iron deficiency; photosynthesis; transcriptome.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
Phenotype of erf109 mutant plants and Col-0 wild-type. (A) Growth (21-day-old plants), (B) Fe concentration, (C) Fv/Fm ratio, (D) quantum yields of PSI, and (E) SPAD value of chlorophyll content of Col-0 and erf109 under Fe sufficiency (Col, erf109) or Fe deficiency (Col-Fe, erf109-Fe). Statistically significant difference was conducted by Student’s t-test at P < 0.05 between either two selected treatment or genotype, marked as asterisk. n.s., no significant; +Fe, iron sufficient condition; –Fe, iron-deficiency treatment. Bar, 5 cm.
FIGURE 2
FIGURE 2
Differentially expressed transcripts, expression profiles and gene ontologies of Col-Fe, the erf109-regulon and erf109-Fe. (A) Heatmap of three transcriptomic profiles. Red and blue color indicates up- and down-regulated expression of DEGs with log2-fold change, respectively. (B) Venn diagram of DEGs from Col-Fe and the erf109-regulon. (C) Venn diagram of DEGs from Col-Fe and erf109-Fe. Distribution of up- and down-regulated DEGs overlapping between Col-Fe and the erf109-regulon (D), overlapping between Col-Fe and erf109-Fe (E), and erf109-regulon DEGs in specific of 1,238 Col-Fe DEGs (F). GO analysis (biological process) of 149 up- (G) and 515 down-regulated DEGs (H) overlapping in the Col-Fe and erf109-regulon data sets. Dot size indicates –log10 (P-value), the log value is labeled with the color bar from 1 to 4.
FIGURE 3
FIGURE 3
Co-expression networks of genes that were differentially expressed between genotypes or treatments. (A) Col-Fe, (B) erf109-regulon, and (C) erf109-Fe. Log2-fold change of DEGs are labeled by color: gray, no significant changes; red, up-regulated; blue, down-regulated.
FIGURE 4
FIGURE 4
Functional visualization of DEGs involved in pathogen defense. (A) Col-Fe, (B) erf109-regulon. Graphs were generated with MapMan software (Thimm et al., 2004). Heatmap depicting log2 fold-changes of the transcription factors (C) and other functional DEGs (D) in group 1. Log2-fold changes of DEGs are labeled by color: white, no significant changes; red, up-regulated, blue: down-regulated.
FIGURE 5
FIGURE 5
Differentially expressed genes encoding photosynthesis-related proteins. (A) Col-Fe, (B) erf109-regulon. Graphs were generated with MapMan software (Thimm et al., 2004). Heatmap depicting log2 fold-changes of genes encoding photosynthesis subunits (C) and genes involved in chlorophyll biosynthesis (D) in group 2. Log2-fold changes of DEGs are labeled by color: white, no significant changes; red, up-regulated; blue, down-regulated.
FIGURE 6
FIGURE 6
Quantitative RT-PCR analysis of relative fold change of Fe-responsive genes in Col-0 and erf109 plants under Fe-sufficient or Fe-deficient conditions. The level of transcript was normalized to Col-0 under Fe-sufficient conditions. Data are presented as mean ± SE from two biological replicates. Student’s t-test significantly different at P < 0.05 is marked with an asterisk.
FIGURE 7
FIGURE 7
Quantitative RT-PCR analysis of relative fold change of DEGs in Col-0 and erf109 under Fe-sufficient (Col, erf109) or Fe-deficient conditions (Col-Fe, erf109-Fe). The level of transcript was normalized to Col-0 under Fe-sufficient conditions. Data are presented as mean ± SE from three biological replicates. Student’s t-test significantly different at P < 0.05 is marked with an asterisk.
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