Elemental profiling and genome-wide association studies reveal genomic variants modulating ionomic composition in Populus trichocarpa leaves

Raphael Ployet; Kai Feng; Jin Zhang; Ivan Baxter; David C Glasgow; Hunter B Andrews; Miguel Rodriguez; Jin-Gui Chen; Gerald A Tuskan; Timothy J Tschaplinski; David J Weston; Madhavi Z Martin; Wellington Muchero

doi:10.3389/fpls.2024.1450646

Elemental profiling and genome-wide association studies reveal genomic variants modulating ionomic composition in Populus trichocarpa leaves

Front Plant Sci. 2024 Nov 28:15:1450646. doi: 10.3389/fpls.2024.1450646. eCollection 2024.

Authors

Raphael Ployet^{1

2}, Kai Feng^{1

2}, Jin Zhang^{1

2}, Ivan Baxter³, David C Glasgow⁴, Hunter B Andrews⁵, Miguel Rodriguez^{1

2}, Jin-Gui Chen^{1

2}, Gerald A Tuskan^{1

2}, Timothy J Tschaplinski^{1

2}, David J Weston^#¹, Madhavi Z Martin^#^{1

2}, Wellington Muchero^#^{1

2}

Affiliations

¹ Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, United States.
² Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, TN, United States.
³ Donald Danforth Plant Science Center, St. Louis, MO, United States.
⁴ Chemical Sciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, United States.
⁵ Radioisotopes Science and Technology Division, Oak Ridge National Laboratory, Oak Ridge, TN, United States.

^# Contributed equally.

Abstract

The ionome represents elemental composition in plant tissues and can be an indicator of nutrient status as well as overall plant performance. Thus, identifying genetic determinants governing elemental uptake and storage is an important goal for breeding and engineering biomass feedstocks with improved performance. In this study, we coupled high-throughput ionome characterization of leaf tissues with high-resolution genome-wide association studies (GWAS) to uncover genetic loci that modulate ionomic composition in leaves of poplar (Populus trichocarpa). Significant agreement was observed across the three ionomic profiling platforms tested: inductively coupled plasma-mass spectrometry (ICP-MS), neutron activation analysis (NAA) and laser-induced breakdown spectroscopy (LIBS). Relative quantification of 20 elements using ICP-MS across a population of 584 genotypes, revealed larger variation in micro-nutrients and trace elements content than for macro-nutrients across genotypes. The GWAS performed using a set of high-density (>8.2 million) single nucleotide polymorphisms, identified over 600 loci significantly associated with variations in these mineral elements, pointing to numerous uncharacterized candidate genes. A significant enrichment for genes related to ion homeostasis and transport was observed, including several members of the cation-proton antiporters (CPA) family and MATE efflux transporters, previously reported to be critical for plant growth and fitness in other species. Our results also included a polymorphic copy of the high-affinity molybdenum transporter MOT1 found directly associated to molybdenum content. For the first time in a perennial plant, our results provide evidence of genetic control of mineral content in a model tree species.

Keywords: GWAS; Populus; ion homeostasis; ionomics; laser-induced breakdown spectroscopy; molybdenum transporter; neutron activation analysis; plasma-mass spectrometry.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This manuscript has been financially supported by the Center for Bioenergy Innovation (CBI), which is a U.S. Department of Energy Bioenergy Research Center supported by the Office of Biological and Environmental Research Program in the DOE Office of Science under Award Number ERKP886. This research used resources of the Compute and Data Environment for Science (CADES) at the Oak Ridge National Laboratory, which is managed by UT‐Battelle, LLC for the Office of Science of the U.S. Department of Energy under Contract Number DE‐AC05‐00OR22725.