Evolutionary flexibility in flooding response circuitry in angiosperms

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Abstract

Flooding due to extreme weather threatens crops and ecosystems. To understand variation in gene regulatory networks activated by submergence, we conducted a high-resolution analysis of chromatin accessibility and gene expression at three scales of transcript control in four angiosperms, ranging from a dryland-adapted wild species to a wetland crop. The data define a cohort of conserved submergence-activated genes with signatures of overlapping cis regulation by four transcription factor families. Syntenic genes are more highly expressed than nonsyntenic genes, yet both can have the cis motifs and chromatin accessibility associated with submergence up-regulation. Whereas the flexible circuitry spans the eudicot-monocot divide, the frequency of specific cis motifs, extent of chromatin accessibility, and degree of submergence activation are more prevalent in the wetland crop and may have adaptive importance.

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Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants

Daniel Gibbs, Seung Cho Lee, Nurulhikma Md Isa … (2011)

Plants and animals are obligate aerobes, requiring oxygen for mitochondrial respiration and energy production. In plants, an unanticipated decline in oxygen availability (hypoxia), as caused by root waterlogging or foliage submergence, triggers changes in gene transcription and mRNA translation that promote anaerobic metabolism and thus sustain substrate-level ATP production 1 . In contrast to animals 2 , oxygen sensing has not been ascribed to a mechanism of gene regulation in response to oxygen deprivation in plants. Here we show that the N-end rule pathway of targeted proteolysis acts as a homeostatic sensor of severe low oxygen in Arabidopsis, through its regulation of key hypoxia response transcription factors. We found that plants lacking components of the N-end rule pathway constitutively express core hypoxia response genes and are more tolerant of hypoxic stress. We identify the hypoxia-associated Ethylene Response Factor (ERF) Group VII transcription factors of Arabidopsis as substrates of this pathway. Regulation of these proteins by the N-end rule pathway occurs through a characteristic conserved motif at the N-terminus initiating with MetCys- (MC-). Enhanced stability of one of these proteins, HRE2, under low oxygen conditions improves hypoxia survival and reveals a molecular mechanism for oxygen sensing in plants via the evolutionarily conserved N-end rule pathway. SUB1A-1, a major determinant of submergence tolerance in rice 3 , was shown not to be a substrate for the N-end rule pathway despite containing the N-terminal motif, suggesting that it is uncoupled from N-end rule pathway regulation, and that enhanced stability may relate to the superior tolerance of Sub1 rice varieties to multiple abiotic stresses 4 .

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Flood adaptive traits and processes: an overview.

Laurentius Voesenek, Julia Bailey-Serres (2015)

Unanticipated flooding challenges plant growth and fitness in natural and agricultural ecosystems. Here we describe mechanisms of developmental plasticity and metabolic modulation that underpin adaptive traits and acclimation responses to waterlogging of root systems and submergence of aerial tissues. This includes insights into processes that enhance ventilation of submerged organs. At the intersection between metabolism and growth, submergence survival strategies have evolved involving an ethylene-driven and gibberellin-enhanced module that regulates growth of submerged organs. Opposing regulation of this pathway is facilitated by a subgroup of ethylene-response transcription factors (ERFs), which include members that require low O₂ or low nitric oxide (NO) conditions for their stabilization. These transcription factors control genes encoding enzymes required for anaerobic metabolism as well as proteins that fine-tune their function in transcription and turnover. Other mechanisms that control metabolism and growth at seed, seedling and mature stages under flooding conditions are reviewed, as well as findings demonstrating that true endurance of submergence includes an ability to restore growth following the deluge. Finally, we highlight molecular insights obtained from natural variation of domesticated and wild species that occupy different hydrological niches, emphasizing the value of understanding natural flooding survival strategies in efforts to stabilize crop yields in flood-prone environments.

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How to usefully compare homologous plant genes and chromosomes as DNA sequences.

Eric Lyons, Michael Freeling (2008)

There are four sequenced and publicly available plant genomes to date. With many more slated for completion, one challenge will be to use comparative genomic methods to detect novel evolutionary patterns in plant genomes. This research requires sequence alignment algorithms to detect regions of similarity within and among genomes. However, different alignment algorithms are optimized for identifying different types of homologous sequences. This review focuses on plant genome evolution and provides a tutorial for using several sequence alignment algorithms and visualization tools to detect useful patterns of conservation: conserved non-coding sequences, false positive noise, subfunctionalization, synteny, annotation errors, inversions and local duplications. Our tutorial encourages the reader to experiment online with the reviewed tools as a companion to the text.