Apoplastic hydrogen peroxide in the growth zone of the maize primary root. Increased levels differentially modulate root elongation under well-watered and water-stressed conditions

Authors: VOOTHULURU, PRIYAMVADA - University Of Missouri; MAKELA, PIRJO - University Of Helsinki; ZHU, JINMING - University Of Missouri; YAMAGUCHI, MINEO - University Of Missouri; Cho, In-Jeong; Oliver, Melvin; SIMMONDS, JOHN - Agriculture And Agri-Food Canada; SHARP, ROBERT - University Of Missouri

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/18/2020
Publication Date: 4/21/2020
Citation: Voothuluru, P., Makela, P., Zhu, J., Yamaguchi, M., Cho, I., Oliver, M.J., Simmonds, J., Sharp, R.E. 2020. Apoplastic hydrogen peroxide in the growth zone of the maize primary root. Increased levels differentially modulate root elongation under well-watered and water-stressed conditions. Plant, Cell & Environment. 11: Article 392. https://doi.org/10.3389/fpls.2020.00392.
DOI: https://doi.org/10.3389/fpls.2020.00392

Interpretive Summary: As the scientific community continues to strive for novel strategies to improve drought tolerance in major crops there has been a growing interest in understanding mechanisms by which roots maintain growth under severe soil moisture deficits (drought). Previous work had demonstrated that under drought cellular elongation (one aspect of growth) is maintained in the tip region of the root growth zone but progressively inhibited further from the apex, and that the rate of cell production (the second aspect of growth) is also decreased. We had also determined that hydrogen peroxide increased in the spaces between cells in the apical region of the root when the roots were under drought conditions and that the hydrogen peroxide was generated by the activity of a root enzyme, oxalate oxidase (OA). Using transgenic plants that constitutively express OA we were able to demonstrate that under well-watered conditions the hydrogen peroxide generated outside the cells positively influenced cell elongation but under drought the effect was the opposite (negative). Moreover, under well watered conditions the effect of the hydrogen peroxide was the result of an increase in both cell proliferation and cell elongation. However, under drought, when hydrogen peroxide levels increase, there is a decrease in cell production and thus growth is slowed. These in-depth physiological discoveries concerning how roots grow under drought conditions will lead to not only a better understanding of root biology but also provide novel strategies for influencing root growth under drought in crop improvement efforts.

Technical Abstract: Reactive oxygen species (ROS) can act as signaling molecules involved in the acclimation of plants to various abiotic and biotic stresses. However, it is not clear how the generalized increases in ROS and downstream signaling events that occur in response to stressful conditions are coordinated to modify plant growth and development. Previous studies of maize (Zea mays L.) primary root growth under water deficit stress showed that cell elongation is maintained in the apical region of the growth zone but progressively inhibited further from the apex, and that the rate of cell production is also decreased. It was observed that apoplastic ROS, particularly hydrogen peroxide (H2O2), increased specifically in the apical region of the growth zone under water stress, resulting at least partly from increased oxalate oxidase activity in this region. To assess the function of the increase in apoplastic H2O2 in root growth regulation, transgenic maize lines constitutively expressing a wheat oxalate oxidase were utilized in combination with kinematic growth analysis to examine effects of increased apoplastic H2O2 on the spatial pattern of cell elongation and on cell production in well-watered and water-stressed roots. Effects of H2O2 removal (via scavenger pretreatment) specifically from the apical region of the growth zone were also assessed. The results show that apoplastic H2O2 positively modulates cell production and root elongation under well-watered conditions, whereas the normal increase in apoplastic H2O2 in water-stressed roots is causally related to down-regulation of cell production and root growth inhibition. The effects on cell production were accompanied by changes in spatial profiles of cell elongation and in the length of the growth zone. However, effects on overall cell elongation, as reflected in final cell lengths, were minor. These results reveal a fundamental role of apoplastic H2O2 in regulating cell production and root elongation in both well-watered and water-stressed conditions.