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

Chiu-Ling Yang,Patricia Klein,I-Chun Pan,Ming-Tsair Chan,Wolfgang Schmidt,Yu-Ting Huang

doi:10.3389/fpls.2022.841366

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.

Highlights

By virtue of its ability to change valency, iron (Fe) is a critical component of photosynthesis and respiratory electron transport, a constituent of Fe-sulfur clusters, and a cofactor of a multitude of vital redox enzymes
149 upregulated differentially expressed genes (DEGs) are involved in the response to abiotic stimulus and cellular nitrogen compound metabolism (Figure 2G), and 515 down-regulated DEGs are associated with the response to biotic stimulus, wounding, chitin, and the immune system (Figure 2H). These results indicate that knock-out of ETHYLENE-RESPONSIVE TRANSCRIPTION FACTOR109 (ERF109) induces gene expression patterns that were to a large part similar to those observed in Fe-deficient wild-type plants and predicted to be involved in establishing immunity
The highly similar transcriptome expression patterns of Fe-sufficient erf109 mutants and Fe-deficient wild-type plants suggest that ERF109 is an upstream regulator of the Fe deficiency-induced immunity response

Summary

Introduction

By virtue of its ability to change valency, iron (Fe) is a critical component of photosynthesis and respiratory electron transport, a constituent of Fe-sulfur clusters, and a cofactor of a multitude of vital redox enzymes. Owing to the chemical characteristic of Fe, free Fe ions in plant cells are highly redox active and can react with H2O2 to produce the reactive hydroxyl (·OH) radical in the so-called Fenton reaction, which can cause oxidative stress and cell damage when produced in excess (Floyd and Lewis, 1983; Baker and Gebicki, 1986). Similar to Fe deficiency, high levels of light irradiation cause oxidative stress in plant cells (Erickson et al, 2015). When the light intensity exceeds the photosynthetic capacity of the plant, excessive energy can induce light inhibition of photosynthesis and cause the formation of excessive ROS species, resulting in leaf cell death (Karpinski et al, 2013). Systemic Acquired Acclimation (SAA) is induced by the exposure of leaves to high light stress, which triggers systemic signaling and preacclimation of shaded leaves (Rossel et al, 2007)

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Discussion

Conclusion