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Research Project: Applied Agricultural Genomics and Bioinformatics Research

Location: Genomics and Bioinformatics Research

Title: Liguleless narrow and narrow odd dwarf act in overlapping pathways to regulate maize development & physiology

Author
item ABRAHAM-JUAREZ, MARIA - National Laboratory Of Genomics And Biodiversity
item BUSCHE, MICHAEL - University Of Wisconsin
item ANDERSON, ALYSSA - University Of California
item LUNDE, CHINA - University Of California
item Winders, Jeremy
item CHRISTENSEN, SHAWN - Brigham Young University
item Hunter, Charles
item Hake, Sarah
item BRUNKARD, JACOB - University Of Wisconsin

Submitted to: The Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/5/2022
Publication Date: 9/27/2022
Citation: Abraham-Juarez, M.J., Busche, M., Anderson, A.A., Lunde, C., Winders, J.R., Christensen, S.A., Hunter Iii, C.T., Hake, S.C., Brunkard, J.O. 2022. Liguleless narrow and narrow odd dwarf act in overlapping pathways to regulate maize development & physiology. The Plant Journal. https://doi.org/10.1111/tpj.15988.
DOI: https://doi.org/10.1111/tpj.15988

Interpretive Summary: As plants develop through their life span, they must balance their energy between growth and defense against attacking pests and pathogens. The “growth-defense trade-offs” are observed through a shift in plants metabolism. Growth (primary) metabolism is temporally halted while stress defense (secondary) metabolism is ramped up to protect the plant. Deciphering how these complex signaling pathways intersect and diverge is a major goal for plant biology, especially in agricultural crops, where breeding robust and resilient crop plants that can withstand stresses without sacrificing yields. This study investigates the growth-defense trade-off relationship on leaf development using two mutant maize genotypes. The mutants, Liguleless narrow (LGN) and narrow odd dwarf (NOD), encode membrane proteins that cause developmental defects in leaf growth. To study the development and immunity impacts of NOD and LGN a range of biochemical, molecular, cellular, genetic, genomic, and metabolomic approaches were employed to investigate potential interacting proteins. We discovered large overlaps between the NOD and LGN signaling pathways. Furthermore, we demonstrated that NOD and LGN act through overlapping pathways to impact maize physiology and development. To our surprise, we identified a potential NOD-interacting protein that is part of a mechanical sensing channel of calcium. Many of the growth metabolites were observed to decrease. In contrast, defense metabolites increased in abundance due to increased stress signaling. Using unbiased profiling approaches to define molecular phenotypes of the single and double mutants, we found that the maize biology is reprogram to promote stress and pathogen defense responses at the cost of reducing resources allocated to growth and development, an illustration of the “growth-defense trade-off” hypothesis.

Technical Abstract: The narrow odd dwarf (nod) and Liguleless narrow (Lgn) are both pleiotropic maize mutants that encode plasma membrane proteins which cause similar developmental patterning defects, and constitutively induce stress signaling pathways. To investigate how these mutants coordinate maize development and physiology, we screened for protein interactors of NOD by affinity purification. LGN was identified by this screen as a strong candidate interactor, and we confirmed the NOD-LGN molecular interaction through orthogonal experiments. We further demonstrated that LGN, a receptor-like kinase, can phosphorylate NOD in vitro, hinting that they could act in intersecting signal transduction pathways. To test this hypothesis, we generated Lgn-R;nod mutants in two backgrounds (B73 and A619) and found that these mutations enhance each other, causing more severe developmental defects than either single mutation on its own, with phenotypes including very narrow leaves, increased tillering, and failure of the main shoot. Transcriptomic and metabolomic analyses of the single and double mutants in the two genetic backgrounds revealed widespread induction of pathogen defense genes and a shift in resource allocation away from primary metabolism in favor of specialized metabolism. These effects were similar in each single mutant and heightened in the double mutant, leading us to conclude that NOD and LGN act cumulatively in overlapping signaling pathways to coordinate growth-defense tradeoffs in maize.