Making sense of low oxygen sensing

TLDR: It is proposed that the turnover of group VII ERFs is of ecological relevance in wetland species and might be manipulated to improve flood tolerance of crops and evade oxygen-regulated N-end rule degradation.

About: This article is published in Trends in Plant Science.The article was published on 2012-03-01 and is currently open access. It has received 456 citations till now.

Figures

Figure 1. Numbers of floods have increased in each of the past six decades across the globe. Graphs show the number of floods classified as a disaster in the International Disaster Database of the University of Louvain, Belgium for the period from 1950 through 2009 by geographical region [93]. Events include river or coastal floods, rapid snow melts, heavy rainfall and other occurrences that caused significant social or economic hardship. Adapted from a Millennium Ecosystem Assessment map (http:// maps.grida.no/go/graphic/number-of-flood-events-by-continent-and-decade-since-1950).

Figure 3. Oxygen sensing via N-end rule pathway-targeted turnover of group VII ERFs. (a) N terminal alignment of Arabidopsis group VII ERFs. With the exception of SUB1C, all begin with the amino acids ‘Met-Cys’ (MC). The highly conserved Arabidopsis N terminal motif is boxed in red and is less conserved in the proteins at loci associated with submergence responses in rice. (b) Homeostatic response to hypoxia is regulated by the N-end rule-mediated proteolysis of group VII ERFs in Arabidopsis. Group VII ERF transcription factors are either constitutively expressed and/or differentially transcriptionally regulated in response to variable signals, including low O2, ethylene and darkness. Four of the five ERFs (HRE1, HRE2, RAP2.2 and RAP2.12) have been implicated in the regulation of hypoxia-responsive genes. Under oxygen-replete conditions (normoxia), ERFs are degraded via the Nend rule pathway of proteolysis. This involves the following steps: (i) the N terminal Met (M) is constitutively cleaved by a methionine aminopeptidase (MAP); (ii) the exposed Cys (C) is converted to an oxidized (C*) form (e.g. Cys-sulfonic acid) by O2, NO or possibly ROS; (iii) an Arg (R) residue is added to the oxidized

Table 1. Factors that contribute to survival of flooding or oxygen deprivation

Figure 2. Metabolic reconfiguration under low oxygen stress. Reduced oxygen availability alters metabolism to maximize substrate level ATP production. The model depicts the major known changes that include enhanced sucrose–starch metabolism, glycolysis, fermentation, a modified tricarboxylic acid (TCA) flow, an alanine and 2- oxoglutarate (2OG) shunt and a g-aminobutyric acid (GABA) shunt. The hypothesis that oxygen is conserved is under further investigation. Yellow boxes summarize notable metabolic adjustments. Blue lines indicate pathways enhanced during the stress, blue dashed lines indicate pathways proposed to be active during the stress and gray dashed lines indicate reactions that are inhibited during the stress. Metabolites that increase during the stress are shown in enlarged black font; metabolites that decrease are shown in red font. Abbreviations are as follows: 2OG, 2-oxoglutarate; ADH, alcohol dehydrogenase; GAD, glutamic acid decarboxylase; GDH, glutamate dehydrogenase, INV, invertase; LDH, lactate dehydrogenase; MDH, malate dehydrogenase; PDC, pyruvate decarboxylase; SCS, succinyl CoA ligase; SUS, sucrose synthase.

Frequently asked questions

Q1. What are the contributions in "Making sense of low oxygen sensing" ?

In this paper, the authors proposed a method for plant cell biology and plant ecophysiology based on gene expression. 

Q2. What is the effect of SUB1A-1 on the re-establishment?

(5) SUB1A-1 enhances upregulation of genes associated with reactive oxygen species (ROS) amelioration and survival of dehydration, thereby improving re-establishment following de-submergence [32]. 

Q3. What is the mechanism of the oxidation of Cys2?

When oxygen becomes limiting (hypoxia), degradation of the ERFs by the N-end rule pathway is inhibited due to a lack of oxygen-mediated Cys2 oxidation. 

Q4. What is the degree of oxygen deficiency?

The degree of oxygen deficiency (hypoxia/anoxia) depends on multiple factors including replenishment of oxygen through photosynthesis, inward diffusion from the water layer and cellular consumption of oxygen through metabolic activity. 

Q5. What is the effect of waterlogging on the root and aerial portions of a plant?

When both the root and aerial portions of a plant are whelmed by water – a condition termed submergence – cellular oxygen levels can also decline from normoxia. 

Q6. How can the authors improve crop resilience to water extremes?

improvement of crop resilience to water extremes can be accomplished by harnessing natural genetic diversity in breeding programs. 

Q7. What is the mechanism of direct oxygen sensing in animals?

In animals, direct oxygen sensing regulates the accumulation of the a subunit of the hypoxia inducible factor (HIF) 1a/b transcription factor [58]. 

Q8. What is the N-end rule pathway of targeted proteolysis?

The conserved N-end rule pathway of targeted proteolysis regulates the half-life of certain cellular proteins based onrecognition of N terminal residues by specific N-recognin E3 ligases [68]. 

Q9. What is the AP2 binding domain in the plant ERF family?

The plant-specific ERF transcription factor family includes over 100 members in rice and Arabidopsis, all of which share an APETALA2 (AP2) DNA binding domain [59]. 

Q10. What genes are involved in regulating the sequestration of mRNAs?

Based on evidence from other eukaryotes, the sequestration of a subset of cellular mRNAs, such as the abundant cohort that encodes ribosomal proteins and translation factors, could be regulated through SnRK1s and the Target of Rapamycin kinase [53]. 

Q11. What is the role of ethylene in the response to submergence?

Ethylene initiates submergence survival strategies in rice and wetland species Recent work has exposed mechanisms of response to submergence that center on growth management. 

Q12. What is the significance of the Nend rule in regulating the abundance of group VII ERF?

Given the crucial importance of modulation of energy reserves during flooding, it is not surprising that variation of group VII ERF susceptibility to oxygen-dependent Nend rule turnover exists in nature. 

Q13. What is the role of a-amylases in plant growth?

This signal transduction upregulates transcription of genes encoding a-amylases, which drive catabolism of starch in the seed needed to fuel underwater shoot growth. 

Q14. What is the effect of waterlogging on the root systems of rice?

The flooding of root systems – a condition termed waterlogging – has little or no impact in semi-aquatic species such as rice that constitutively form gas conduits (i.e. aerenchyma) between submerged and aerial organs. 

Q15. What is the reason for the absence of PRT6 or ATE activity?

the absence of PRT6 or ATE activity may enhance anaerobic metabolism to prolong survival in sucrose-fed seedlings but may cause a more rapid onset of energy deficiency in submerged plants. 

Q16. What is the likely explanation for the stability of group VII ERFs under hypoxia?

Based on this evidence, the stabilization of group VII ERFs under hypoxia is most probably related to an inhibition of the Cys2 oxidation that is required before the protein can be arginylated and degraded. 

Q17. What is the role of the group VII ERFs in the regulation of hypoxia?

Several recent reports indicate that Arabidopsis group VII ERFs redundantly regulate hypoxia-responsive gene expression and survival of low oxygen stress. 

Q18. What is the role of the N-end rule pathway in regulating the accumulation of group VII?

the N-end rule pathway (i) prevents the excessive accumulation of constitutively expressed ERFs under normoxia; (ii) allows for stabilization of both constitutive and induced ERFs during hypoxia; and (iii) facilitates rapid reversal of ERF-regulated transcription upon reoxygenation. 

Q19. What is the role of pyruvate in anaerobic metabolism?

metabolism of pyruvate to alanine provides an alternative, non-detrimental end product of anaerobic metabolism that is observed in a number of species [17,18]. 

Q20. What are the biological determinants of the two flooding survival strategies?

The genetic determinants and hormonal signaling pathways that underlie the two flooding survival strategies have been identified.