Acetic acid positively modulates proline metabolism for mitigating PEG-mediated drought stress in Maize and Arabidopsis

Sakil Mahmud; Mohammad Kamruzzaman; Sabarna Bhattacharyya; Khadiga Alharbi; Diaa Abd El Moneim; Mohammad Golam Mostofa

doi:10.3389/fpls.2023.1167238

Acetic acid positively modulates proline metabolism for mitigating PEG-mediated drought stress in Maize and Arabidopsis

Front Plant Sci. 2023 Jul 19:14:1167238. doi: 10.3389/fpls.2023.1167238. eCollection 2023.

Authors

Sakil Mahmud¹, Mohammad Kamruzzaman^{2

3}, Sabarna Bhattacharyya⁴, Khadiga Alharbi⁵, Diaa Abd El Moneim⁶, Mohammad Golam Mostofa^{7

8}

Affiliations

¹ Department of Biochemistry and Molecular Biology, Bangladesh Agricultural University, Mymensingh, Bangladesh.
² Department of Plant Breeding, Institute of Crop Science and Resource Conservation, University of Bonn, Bonn, Germany.
³ Plant Breeding Division, Bangladesh Institute of Nuclear Agriculture (BINA), Mymensingh, Bangladesh.
⁴ Plant Cell Biology, Institute of Cellular and Molecular Botany, University of Bonn, Bonn, Germany.
⁵ Department of Biology, College of Science, Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia.
⁶ Department of Plant Production (Genetic Branch), Faculty of Environmental Agricultural Sciences, Arish University, El-Arish, Egypt.
⁷ Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI, United States.
⁸ Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI, United States.

Abstract

Introduction: Osmotic imbalance is one of the major consequences of drought stress, negatively affecting plant growth and productivity. Acetic acid has modulatory roles in osmotic balance in plants; however, the mechanistic insights into acetic acid-mediated osmotic adjustment under drought stress remains largely unknown.

Methods: Here, we investigated how seed priming and seedling root treatment with acetic acid enabled maize plants overcoming polyethylene glycol (PEG)-induced drought effects.

Results: Maize seeds primed with acetic acid showed better growth performance when compared with unprimed seeds under PEG application. This growth performance was mainly attributed to improved growth traits, such as fresh weight, dry weight, length of shoots and roots, and several leaf spectral indices, including normalized difference vegetation index (NDVI) and chlorophyll absorption in reflectance index (MCARI). The levels of oxidative stress indicators hydrogen peroxide (H₂O₂) and malondialdehyde (MDA) did not alter significantly among the treatments, but proline content as well as the expression of proline biosynthetic gene, Δ1-PYRROLINE-5-CARBOXYLATE SYNTHETASE 1 (P5CS1) was significantly elevated in plants receiving acetic acid under PEG-treatments. On the other hand, treating the seedlings root with acetic acid led to a significant recovery of maize plants from drought-induced wilting. Although growth traits remained unchanged among the treatments, the enhancement of leaf water content, photosynthetic rate, proline level, expression of P5CS1, and antioxidant enzyme activities along with reduced level of H₂O₂ and MDA in acetic acid-supplemented drought plants indicated a positive regulatory role of acetic acid in maize tolerance to drought. Moreover, the high expression of P5CS1 and the subsequent elevation of proline level upon acetic acid application were further validated using wild type and proline biosynthetic mutant p5cs1 of Arabidopsis. Results showed that acetic acid application enabled wild type plants to maintain better phenotypic appearance and recovery from drought stress than p5cs1 plants, suggesting a crosstalk between acetic acid and proline metabolism in plants under drought stress.

Discussion: Our results highlight the molecular and intrinsic mechanisms of acetic acid conferring plant tolerance to drought stress.

Keywords: acetic acid; antioxidant defense; maize (Zea mays L.); osmotic stress; proline metabolism.

Grants and funding

This research was funded by Princess Nourah bint Abdulrahman University Researchers Supporting Project number (PNURSP2023R188), Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia. We also gratefully acknowledge the financial support from the National Agricultural Technology Project (NATP), Phase-II, PIU, Bangladesh Agricultural Research Council to MK for this research outcome.