Evolutionary flexibility in flooding response circuitry in angiosperms

Reynoso, Mauricio; Kajala, Kaisa; Bajic, Marko; West, Donnelly A.; Pauluzzi, Germain; Yao, Andrew I.; Hatch, Kathryn F.; Zumstein, Kristina; Woodhouse, Margaret R.; Rodriguez‐Medina, Joel; Sinha, Neelima; Brady, Siobhán M.; Deal, Roger B.; Bailey‐Serres, Julia

doi:10.1126/science.aax8862

Cited by 128 publications

(159 citation statements)

References 70 publications

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“…Non-symbiotic hemoglobins are induced in root exposed to hypoxic stress and are involved in NO scavenging leading to the formation of nitrosyl-phytoglobins after interaction with NO 58,59 . Moreover, it has been shown that overexpression of PGB1 in A. thaliana enhances hypoxia tolerance and post-hypoxia survival 60 . Figure 8.…”

Section: Hypoxia-induced Ros Production Redox Associated Gene Expresmentioning

confidence: 99%

RNA-Seq reveals novel genes and pathways associated with hypoxia duration and tolerance in tomato root

Safavi-Rizi

Herde

Stöhr

2020

Sci Rep

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Due to climate change, economically important crop plants will encounter flooding periods causing hypoxic stress more frequently. this may lead to reduced yields and endanger food security. As roots are the first organ to be affected by hypoxia, the ability to sense and respond to hypoxic stress is crucial. At the molecular level, therefore, fine-tuning the regulation of gene expression in the root is essential for hypoxia tolerance. Using an RnA-Seq approach, we investigated transcriptome modulation in tomato roots of the cultivar 'Moneymaker', in response to short-(6 h) and long-term (48 h) hypoxia. Hypoxia duration appeared to have a significant impact on gene expression such that the roots of five weeks old tomato plants showed a distinct time-dependent transcriptome response. We observed expression changes in 267 and 1421 genes under short-and long-term hypoxia, respectively. Among these, 243 genes experienced changed expression at both time points. We identified tomato genes with a potential role in aerenchyma formation which facilitates oxygen transport and may act as an escape mechanism enabling hypoxia tolerance. Moreover, we identified differentially regulated genes related to carbon and amino acid metabolism and redox homeostasis. Of particular interest were the differentially regulated transcription factors, which act as master regulators of downstream target genes involved in responses to short and/or long-term hypoxia. Our data suggest a temporal metabolic and anatomic adjustment to hypoxia in tomato root which requires further investigation. We propose that the regulated genes identified in this study are good candidates for further studies regarding hypoxia tolerance in tomato or other crops.

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Section: Hypoxia-induced Ros Production Redox Associated Gene Expresmentioning

confidence: 99%

RNA-Seq reveals novel genes and pathways associated with hypoxia duration and tolerance in tomato root

Safavi-Rizi

Herde

Stöhr

2020

Sci Rep

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“…Contrastingly, but similar to Arabidopsis, R. palustris uses the ethylene signal to promote hypoxia survival and this corresponded with PGB1, RAP2.12 and hypoxia adaptive transcript induction [9]. Finally, natural variation for higher flooding tolerance is frequently found to be correlated with enhanced ethylene signaling [30,31], PGB1 levels and NO removal [32,33], ERFVII levels [31,34] and hypoxia adaptive gene transcripts [30,[35][36][37][38] in crop and ornamental plant species. Taken together, the mechanism of ethylene-mediated hypoxia tolerance could be instrumental in enhancing flooding tolerance of intolerant crops through the manipulation of ethylene responsiveness of PGB1 and ERFVII genes and its downstream signaling targets.…”

Section: Introductionmentioning

confidence: 97%

“…However, whether ethylene also contributes to metabolic hypoxia acclimation and if this correlates with flooding tolerance in these Solanum species is currently unknown. Several studies showed that genes involved in ethylene signaling and ethanolic fermentation are induced in response to flooding and hypoxia, but not consistently across all plant tissues in these Solanum species [37,40,41,45,46].…”

Section: Introductionmentioning

confidence: 99%

Ethylene Differentially Modulates Hypoxia Responses and Tolerance across Solanum Species

Hartman

Dongen

Renneberg

et al. 2020

Plants

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The increasing occurrence of floods hinders agricultural crop production and threatens global food security. The majority of vegetable crops are highly sensitive to flooding and it is unclear how these plants use flooding signals to acclimate to impending oxygen deprivation (hypoxia). Previous research has shown that the early flooding signal ethylene augments hypoxia responses and improves survival in Arabidopsis. To unravel how cultivated and wild Solanum species integrate ethylene signaling to control subsequent hypoxia acclimation, we studied the transcript levels of a selection of marker genes, whose upregulation is indicative of ethylene-mediated hypoxia acclimation in Arabidopsis. Our results suggest that ethylene-mediated hypoxia acclimation is conserved in both shoots and roots of the wild Solanum species bittersweet (Solanum dulcamara) and a waterlogging-tolerant potato (Solanum tuberosum) cultivar. However, ethylene did not enhance the transcriptional hypoxia response in roots of a waterlogging-sensitive potato cultivar, suggesting that waterlogging tolerance in potato could depend on ethylene-controlled hypoxia responses in the roots. Finally, we show that ethylene rarely enhances hypoxia-adaptive genes and does not improve hypoxia survival in tomato (Solanum lycopersicum). We conclude that analyzing genes indicative of ethylene-mediated hypoxia acclimation is a promising approach to identifying key signaling cascades that confer flooding tolerance in crops.

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“…RNA visualization methods that can resolve single RNA molecules and RNA-protein complexes, are a new frontier in plant biology. This particular method is timely given that genomic technologies that monitor RNAPII activity and nascent RNA synthesis uncover modulation of transcript termination and nuclear export (Hetzel et al, 2016;Palovaara et al, 2017;Reynoso et al, 2018;Zhu et al, 2018;Lee and Bailey-Serres, 2019;Reynoso et al, 2019).…”

Section: Location and Relocation: Rna Movement Visualizationmentioning

confidence: 99%

The Dynamic Kaleidoscope of RNA Biology in Plants

2020

Self Cite

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ACKNOWLEDGMENTSWe thank all of the authors, reviewers, and editors, especially Sarah M. Assmann, who contributed to this Focus Issue. We thank Thanin Chantarachot and Sarah M. Assmann for comments on this editorial. LITERATURE CITEDArribas-Hernández L, Brodersen P (2020) Occurrence and functions of m 6 A and other covalent modifications in plant mRNA. Plant Physiol 182: 79-96 Bai B, van der Horst S, Cordewener J, America T, Hanson J, Bentsink L (2020) Seed stored mRNAs that are specifically associated to monosome are translationally regulated during germination. Plant Physiol 182: 378-392 Beck J, Lohscheider JN, Albert S, Andersson U, Mendgen KW, Rojas-Stütz MC, Adamska I, Funck D (2017) Small one-helix proteins are essential for photosynthesis in Arabidopsis. Front Plant Sci 8: 7 Bentley DL (2005) Rules of engagement: Co-transcriptional recruitment of pre-mRNA processing factors. Curr Opin Cell Biol 17: 251-256 Borges F, Martienssen RA (2015) The expanding world of small RNAs in plants. Nat Rev Mol Cell Biol 16: 727-741 Browning KS, Bailey-Serres J (2015) Mechanism of cytoplasmic mRNA translation. The Arabidopsis Book 13: e0176 Cao Y, Ma L (2019) To splice or to transcribe: SKIP-mediated environmental fitness and development in plants. Front Plant Sci 10: 1222 Chantarachot T, Bailey-Serres J (2018) Polysomes, stress granules, and processing bodies: A dynamic triumvirate controlling cytoplasmic mRNA fate and function. Plant Physiol 176: 254-269 Chaudhary S, Khokhar W, Jabre I, Reddy ASN, Byrne LJ, Wilson CM, Syed NH (2019) Alternative splicing and protein diversity: Plants versus animals. Front Plant Sci 10: 708 Crisp PA, Hammond R, Zhou P, Vaillancourt B, Lipzen AM, Daum C, Barry KW, de Leon N, Buell CR, Kaeppler SM, et al (2020) Variation and inheritance of small RNAs in maize inbreds and F1 hybrids. Plant

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Evolutionary flexibility in flooding response circuitry in angiosperms

Cited by 128 publications

References 70 publications

RNA-Seq reveals novel genes and pathways associated with hypoxia duration and tolerance in tomato root

RNA-Seq reveals novel genes and pathways associated with hypoxia duration and tolerance in tomato root

Ethylene Differentially Modulates Hypoxia Responses and Tolerance across Solanum Species

The Dynamic Kaleidoscope of RNA Biology in Plants

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