Oxygen Binding Kinetics and Coordination States of Hemoglobins from Early Land Plants

Sep 29, 2026

Bryophytes—mosses, hornworts, and liverworts—are early-diverging land plants whose hemoglobin genes have largely remained functionally unexplored. Phylogenetic analysis places bryophyte globins as a distinct monophyletic group, equally distant from class 1 and class 2 nonsymbiotic hemoglobins of vascular plants. Spectroscopy shows predominant hexacoordination in the ferrous deoxy state, inconsistent with efficient oxygen transport, yet kinetics reveal oxygen binding and dissociation rates similar to oxygen-transporting leghemoglobins, suggesting alternative physiological roles.

LanguageEnglish

CategoryResearch & Report

FormatPDF

Pages10

Reading Time25 min

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Abstract

Introduction

Plant hemoglobin diversity and evolutionary context

Functional roles of nonsymbiotic hemoglobins

Evolutionary history and research motivation

This article is licensed under CC-BY 4.0 [http://pubs.acs.org/journal/acsodf](http://pubs.acs.org/journal/acsodf) Article Oxygen Binding Kinetics and Coordination States of Hemoglobins from Early Land Plants Sydney Dvorak, Jonathan D. Monroe, Kenneth Hanson, and Ryan Sturms* Cite This: ACS Omega 2025, 10, 59675−59684 Read Online | | | | | | | | --- | --- | --- | --- | --- | --- | | ACCESS | Metrics & More | | Article Recommendations | | *sı Supporting Information | ABSTRACT: Bryophytes, comprising mosses (Bryophyta), hornworts (Anthocerotophyta), and liverworts (Marchantiophyta), represent early diverging lineages in land plant evolution. Each of these phyla contains hemoglobin genes whose functional properties remain largely unexplored. Here, we report phylogenetic analysis that confirms that bryophyte globins form a distinct monophyletic group equally distant from both class 1 and class 2 nonsymbiotic hemoglobins of vascular plants. Spectroscopic characterization revealed that all three representative bryophyte hemoglobins exhibit predominant hexacoordination in the ferrous deoxy state. This predominantly hexacoordinate structure and the autooxidation rates, which are similar to other nonsymbiotic hemoglobins, are inconsistent with efficient oxygen transport function. However, kinetic analysis revealed a striking paradox: oxygen binding and dissociation rates closely resembling those of oxygen-transporting leghemoglobins. These findings reveal that bryophyte globins possess the kinetic capacity for rapid oxygen exchange but have structural features, namely, a hexacoordinate heme prosthetic group, that preclude efficient oxygen transport. This suggests that hemoglobins from early land plants served alternative physiological functions and that the inherent oxygen-binding capabilities of the globin fold were later optimized for transport in vascular plant lineages. ■ INTRODUCTION Hemoglobin (Hb) proteins are found across all three domains of life: archaea, bacteria, and eukarya. 1,2 Among eukaryotes, Hbs have been found in both plant and animal lineages.2−4 The first plant Hb to be discovered was the symbiotic leghemoglobin, with nonsymbiotic and truncated hemoglobin being discovered later.5 Previous phylogenetic studies indicate that these plant Hbs have evolved into distinct monophyletic groups. 1,2,4−7 These include leghemoglobins (Lbs), class 1 and 2 nonsymbiotic hemoglobins (nsHbs), and class 3 truncated Hbs. Class 3 truncated Hbs are structurally distinct globins with a 2/2 helical fold rather than the canonical 3/3 fold observed in fulllength globins.8 Furthermore, these analyses have placed bryophyte globins, which are sometimes categorized as class 0 Hbs, distinct from both class 1 and class 2 nsHbs.6 From a functional viewpoint, several decades of work have provided a thorough in vitro analysis of ligand binding and reaction kinetics to understand the varied roles that Hbs play.3,9−20 The oxygen transport function of symbiotic plant Hbs, the leghemoglobins, has been studied in-depth, specifically in their interactions with Rhizobium bacteria in nitrogen-fixing organisms.21 These Hbs are known to facilitate the diffusion of oxygen in infected root nodule cells in support of symbiotic nitrogen fixation.22 The nsHbs, however, do not primarily function to facilitate the diffusion of oxygen.23 Instead, nsHbs have a wide range of hypothesized functions, likely related to nitric oxide (NO) homeostasis, including abiotic stress response,24 NO signaling and scavenging,16,25−27 promoting plant development and symbiosis,27−30 and supporting anaerobic metabolism by functioning as an alternative oxidase.15,25,28,31 The physiological significance of these biochemical functions and their relative importance under different conditions remain active areas of research. The evolutionary history of plants and their hemoglobins isan important context for understanding other physiological roles

FAQs

How are bryophyte globins positioned phylogenetically relative to vascular plant hemoglobins?

They form a distinct monophyletic group, equally distant from class 1 and class 2 nonsymbiotic hemoglobins of vascular plants.

What spectroscopic feature characterizes bryophyte hemoglobins in the ferrous deoxy state?

All representative bryophyte hemoglobins show predominant hexacoordination.

Why do the kinetics and structure of bryophyte globins suggest alternative functions rather than efficient oxygen transport?

Their hexacoordinate structural features would preclude efficient oxygen transport, yet their oxygen binding and dissociation rates resemble those of oxygen-transporting leghemoglobins.

Sep 29, 2026

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