Sugar modulation of anaerobic-response networks in maize root tips

Maria Angelica Sanclemente, Fangfang Ma, Peng Liu, Adriana Della Porta, Jugpreet Singh, Shan Wu, Thomas Colquhoun, Timothy Johnson, Jiahn Chou Guan, Karen E. Koch

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Sugar supply is a key component of hypoxia tolerance and acclimation in plants. However, a striking gap remains in our understanding of mechanisms governing sugar impacts on low-oxygen responses. Here, we used a maize (Zea mays) root-tip system for precise control of sugar and oxygen levels. We compared responses to oxygen (21 and 0.2%) in the presence of abundant versus limited glucose supplies (2.0 and 0.2%). Low-oxygen reconfigured the transcriptome with glucose deprivation enhancing the speed and magnitude of gene induction for core anaerobic proteins (ANPs). Sugar supply also altered profiles of hypoxia-responsive genes carrying G4 motifs (sources of regulatory quadruplex structures), revealing a fast, sugar-independent class followed more slowly by feast-or-famine-regulated G4 genes. Metabolite analysis showed that endogenous sugar levels were maintained by exogenous glucose under aerobic conditions and demonstrated a prominent capacity for sucrose re-synthesis that was undetectable under hypoxia. Glucose abundance had distinctive impacts on co-expression networks associated with ANPs, altering network partners and aiding persistence of interacting networks under prolonged hypoxia. Among the ANP networks, two highly interconnected clusters of genes formed around Pyruvate decarboxylase 3 and Glyceraldehyde-3-phosphate dehydrogenase 4. Genes in these clusters shared a small set of cis-regulatory elements, two of which typified glucose induction. Collective results demonstrate specific, previously unrecognized roles of sugars in low-oxygen responses, extending from accelerated onset of initial adaptive phases by starvation stress to maintenance and modulation of co-expression relationships by carbohydrate availability.

Original languageEnglish
Pages (from-to)295-317
Number of pages23
JournalPlant Physiology
Volume185
Issue number2
DOIs
Publication statusPublished - Feb 2021

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