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Authors: Emese Eysholdt-Derzsó, Bettina Hause, Margret Sauter and Romy R. Schmidt-Schippers.
Plant, Cell & Environment (2024)
Summary Statement: ERFVII pathway actively maintains abscisic acid homoeostasis, enabling a partial control of lateral root development under hypoxic conditions.
Abstract: "Oxygen limitation (hypoxia), arising as a key stress factor due to flooding, negatively affects plant development. Consequently, maintaining root growth under such stress is crucial for plant survival, yet we know little about the root system's adaptions to low-oxygen conditions and its regulation by phytohormones. In this study, we examine the impact of hypoxia and, herein, the regulatory role of group VII ETHYLENE-RESPONSE FACTOR (ERFVII) transcription factors on root growth in Arabidopsis. We found lateral root (LR) elongation to be actively maintained by hypoxia via ERFVII factors, as erfVII seedlings possess hypersensitivity towards hypoxia regarding their LR growth. Pharmacological inhibition of abscisic acid (ABA) biosynthesis revealed ERFVII-driven counteraction of hypoxia-induced inhibition of LR formation in an ABA-dependent manner. However, postemergence LR growth under hypoxia mediated by ERFVIIs was independent of ABA. In roots, ERFVIIs mediate, among others, the induction of ABA-degrading ABA 8′-hydroxylases CYP707A1 expression. RAP2.12 could activate the pCYC707A1:LUC reporter gene, indicating, combined with single mutant analyses, that this transcription factor regulates ABA levels through corresponding transcript upregulation. Collectively, hypoxia-induced adaptation of the Arabidopsis root system is shaped by developmental reprogramming, whereby ERFVII-dependent promotion of LR emergence, but not elongation, is partly executed through regulation of ABA degradation."
Authors: Elena Loreti and Pierdomenico Perata.
Frontiers in Genetics (2023)
Abstract: "In this review, we focus on ethylene transcription factors (ERFs), which are a crucial family of transcription factors that regulate plant development and stress responses. ERFVII transcription factors have been identified and studied in several crop species, including rice, wheat, maize, barley, and soybean. These transcription factors are known to be involved in regulating the plant’s response to low oxygen stress—hypoxia and could thus improve crop yields under suboptimal growing conditions. In rice (Oryza sativa) several ERFVII genes have been identified and characterized, including SUBMERGENCE 1A (SUB1A), which enables rice to tolerate submergence. The SUB1A gene was used in the development of SUB1 rice varieties, which are now widely grown in flood-prone areas and have been shown to improve yields and farmer livelihoods. The oxygen sensor in plants was discovered using the model plant Arabidopsis. The mechanism is based on the destabilization of ERFVII protein via the N-degron pathway under aerobic conditions. During hypoxia, the stabilized ERFVIIs translocate to the nucleus where they activate the transcription of hypoxia-responsive genes (HRGs). In summary, the identification and characterization of ERFVII transcription factors and their mechanism of action could lead to the development of new crop varieties with improved tolerance to low oxygen stress, which could have important implications for global food security."
Authors: Mizuki Murao, Rika Kato, Shuhei Kusano, Rina Hisamatsu, Hitoshi Endo, Yasuki Kawabata, Seisuke Kimura, Ayato Sato, Hitoshi Mori, Kenichiro Itami, Keiko U. Torii, Shinya Hagihara and Naoyuki Uchida.
Plant and Cell Physiology (2023)
Abstract: "Plant seedlings adjust the growth of the hypocotyl in response to surrounding environmental changes. Genetic studies have revealed key players and pathways in hypocotyl growth, such as phytohormones and light signaling. However, because of genetic redundancy in the genome, it is expected that not-yet-revealed mechanisms can be elucidated through approaches different from genetic ones. Here we identified a small compound, HYGIC (HG), that simultaneously induces hypocotyl elongation and thickening, accompanied by increased nuclear size and enlargement of cortex cells. HG-induced hypocotyl growth required the ethylene signaling pathway activated by endogenous ethylene, involving CONSTITUTIVE PHOTOMORPHOGENIC 1, ETHYLENE INSENSITIVE 2, and redundant transcription factors for ethylene responses, ETHYLENE INSENSITIVE 3 (EIN3) and EIN3 LIKE 1. By using EBS:GUS, a transcriptional reporter of ethylene responses based on an EIN3-binding-cis-element, we found that HG treatment ectopically activates ethylene responses at the epidermis and cortex of the hypocotyl. RNA-seq and subsequent gene ontology analysis revealed that a significant number of HG-induced genes are related to responses to hypoxia. Indeed, submergence, a representative environment where the hypoxia response is induced in nature, promoted ethylene-signaling-dependent hypocotyl elongation and thickening accompanied by ethylene responses at the epidermis and cortex, which resembled the HG treatment. Collectively, the identification and analysis of HG revealed that ectopic responsiveness to ethylene promotes hypocotyl growth, and this mechanism is activated under submergence."
Authors: Mohamad Abbas, Gunjan Sharma, Charlene Dambire, Julietta Marquez, Carlos Alonso-Blanco, Karina Proaño and Michael J. Holdsworth.
Nature (2022)
Editor's view: Plants have adapted to grow at specific altitudes by regulating chlorophyll synthesis in response to ambient oxygen concentration, calibrated by altitude-dependent activity of GROUP VII ETHYLENE RESPONSE FACTOR.
Abstract: "Flowering plants (angiosperms) can grow at extreme altitudes, and have been observed growing as high as 6,400 metres above sea level1,2; however, the molecular mechanisms that enable plant adaptation specifically to altitude are unknown. One distinguishing feature of increasing altitude is a reduction in the partial pressure of oxygen (pO2). Here we investigated the relationship between altitude and oxygen sensing in relation to chlorophyll biosynthesis—which requires molecular oxygen3—and hypoxia-related gene expression. We show that in etiolated seedlings of angiosperm species, steady-state levels of the phototoxic chlorophyll precursor protochlorophyllide are influenced by sensing of atmospheric oxygen concentration. In Arabidopsis thaliana, this is mediated by the PLANT CYSTEINE OXIDASE (PCO) N-degron pathway substrates GROUP VII ETHYLENE RESPONSE FACTOR transcription factors (ERFVIIs). ERFVIIs positively regulate expression of FLUORESCENT IN BLUE LIGHT (FLU), which represses the first committed step of chlorophyll biosynthesis, forming an inactivation complex with tetrapyrrole synthesis enzymes that are negatively regulated by ERFVIIs, thereby suppressing protochlorophyllide. In natural populations representing diverse angiosperm clades, we find oxygen-dependent altitudinal clines for steady-state levels of protochlorophyllide, expression of inactivation complex components and hypoxia-related genes. Finally, A. thaliana accessions from contrasting altitudes display altitude-dependent ERFVII activity and accumulation. We thus identify a mechanism for genetic adaptation to absolute altitude through alteration of the sensitivity of the oxygen-sensing system."
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Authors: Jagannath Swain, Vinay Shukla, Francesco Licausi and Kapuganti Jagadis Gupta.
Trends in Plant Science (2024)
Abstract: "Group VII ethylene-responsive factor (ERFVII) transcription factors are crucial for the adaption of plants to conditions that limit oxygen availability. A recent study by Zubrycka et al. reveals new aspects of ERFVII stabilization through the PLANT CYSTEINE OXIDASE (PCO)-N degron pathway and non-autonomous regulation in response to different endogenous and exogenous cues."
Authors: Agata Zubrycka, Charlene Dambire, Laura Dalle Carbonare, Gunjan Sharma, Tinne Boeckx, Kamal Swarup, Craig J. Sturrock, Brian S. Atkinson, Ranjan Swarup, Françoise Corbineau, Neil J. Oldham and Michael J. Holdsworth.
Nature Communications (2023)
Editor's view: Oxygen is essential for plant life. Here the authors define new functions and components of the plant oxygen sensing mechanism providing an understanding of the biochemistry of sensing and physiological responses allowing plant roots to survive in the soil.
Abstract: "Oxygen is a key signalling component of plant biology, and whilst an oxygen-sensing mechanism was previously described in Arabidopsis thaliana, key features of the associated PLANT CYSTEINE OXIDASE (PCO) N-degron pathway and Group VII ETHYLENE RESPONSE FACTOR (ERFVII) transcription factor substrates remain untested or unknown. We demonstrate that ERFVIIs show non-autonomous activation of root hypoxia tolerance and are essential for root development and survival under oxygen limiting conditions in soil. We determine the combined effects of ERFVIIs in controlling gene expression and define genetic and environmental components required for proteasome-dependent oxygen-regulated stability of ERFVIIs through the PCO N-degron pathway. Using a plant extract, unexpected amino-terminal cysteine sulphonic acid oxidation level of ERFVIIs was observed, suggesting a requirement for additional enzymatic activity within the pathway. Our results provide a holistic understanding of the properties, functions and readouts of this oxygen-sensing mechanism defined through its role in modulating ERFVII stability."
Authors: Yiyi Zhang, Yuanfu Xie, Haifan Shi, Yufen Zhuang, Yuan Zheng, Honghui Lin and Huapeng Zhou.
Plant and Cell Physiology (2023)
Abstract: "Floods impose detrimental effects on natural and agro-ecosystems, leading to significant loss of worldwide crop production. Global climate change has even strengthened this situation. Flooding is a continuous process including two stages of submergence and re-oxygenation, and both are harmful to plant growth and development, resulting in a serious decline on crop yield. Therefore, the understanding of plant flooding tolerance and developing flooding-resistant crops are of great significance. Here, we report that the Arabidopsis thaliana (Arabidopsis) R2R3-MYB transcription factor MYB30 participates in plant submergence response through ACS7 by repressing ethylene (ET) biosynthesis. The MYB30 loss-of-function mutant exhibits reduced submergence tolerance with higher level of ET production, whereas the MYB30-overexpressing plant displays enhanced submergence tolerance and repressed ET production. The coding gene of ACC synthase 7 (ACS7) might be a direct target of MYB30 during submergence response. MYB30 binds to the promoter of ACS7 and represses its transcription. ACS7 loss-of-function mutant with defect in ET biosynthesis displays enhanced submergence tolerance, whereas plants overexpressing ACS7 exhibit a submergence-sensitive phenotype. Genetic analysis shows that ACS7 functions downstream of MYB30 both in ET biosynthesis and submergence response. Taken together, our work revealed a novel transcriptional regulation that modulates submergence response in plants."
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