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The development of aerenchyma and its function of oxygen transportation in Syzygium kunstleri grown in hypoxic conditions

SOU, Hong-duck 東京大学 DOI:10.15083/0002002075

2021.10.04

概要

Flooding and waterlogging are one of the environmental stresses on plant. The rate of oxygen diffusion in water is about 104 fold slower than in air, which may inhibit root aerobic respiration. To overcome the problems induced by hypoxic condition, some plants show anatomical and morphological adaptation such as development of aerenchyma and adventitious roots. Aerenchyma is a tissue composed of intercellular gas spaces that makes it possible to internal diffusion of atmospheric O2 from the aerial region of the plant to the submerged root to prevent serious damage to the roots. There are two kinds of aerenchyma, namely, primary and secondary. Primary aerenchyma develops in the primary tissues, especially in the root cortex. In contrast, secondary aerenchyma is a tissue of secondary origin and differentiates from the phellogen, cambium, or pericycle. In woody plant species, the functions of the secondary aerenchyma becomes more important as the cortex, where the primary aerenchyma formed, is collapsed by secondary thickening. Syzygium kunstleri is a species that occurs in the peat swamp forest of Southeast Asia and is known as flood-tolerant species. The purpose of this study is to improve the understanding of adaptive mechanisms of S. kunstleri to flooding environment. In this study, the anatomical developmental processes of primary and secondary aerenchyma in the adventitious roots of S. kunstleri grown in hypoxic conditions were clarified and their function as oxygen transport pathways was confirmed. Chapter 1 describes the background and purpose of this research.

In chapter 2, I clarified how the distribution of primary and secondary aerenchyma changed in adventitious roots using anatomical techniques. Distribution of primary and secondary aerenchyma in roots is considered to be an important factor in understanding their functions. Hydroponic and 0.1% agar medium were used to make a hypoxic environment. 0.1 % agar medium (‘stagnant solution’) was used to prevent convection in medium, thus reduced dissolved oxygen. When S. kunstleri was grown in hydroponic medium and 0.1 % agar medium, adventitious roots developed from the submerged stem near water surface. Surface color of the root gradually varies from white at root tip through light brown to dark brown near the root base. According to the observation of serial transections along the adventitious roots, primary aerenchyma (schizogenous and lysigenous aerenchyma) and secondary aerenchyma were both found in each root. Schizogenous aerenchyma was found near the root tip, where the root surface color was white or light brown. Lysigenous aerenchyma was found throughout the roots except near the root tip, and the root surface color of the portion found was light brown or dark brown. Periderm with intercellular space, i.e. the secondary aerenchyma, was observed to be large in the root base and smaller toward the root tip. The presence of both primary aerenchyma and secondary aerenchyma were confirmed irrespective of oxygen concentration in medium, and the color of the roots was found to correspond with the respective aerenchyma types. That is, aerenchyma was developed in order of age of tissue within a single root. Yet, the periderm with secondary aerenchyma was more developed in the dark brown part of the roots grown in the agar medium than in the roots grown hydroponic medium. Thus, it is thought that the concentration of oxygen in medium affects the development of secondary aerenchyma in adventitious roots. Since primary and secondary aerenchyma are developed in the cortex and periderm, respectively, the proportion of cortex and periderm implies the development of primary and secondary aerenchyma, respectively. Thus, as the area ratio of cortex decreases while the area ratio of periderm increases, tissues that support the function of primary aerenchyma as an internal O2 pathway can be considered as secondary aerenchyma.

In chapter 3, the function of oxygen transportation in primary and secondary aerenchyma developed in the adventitious roots was confirmed and their continuity also clarified. I examined oxygen dynamics using Clark-type oxygen microelectrodes according to each developmental stage of aerenchyma. The oxygen transport function of primary aerenchyma developed in the adventitious roots was confirmed by a series of pO2 (partial pressure of oxygen) measurement at different positions along the root. As a result of measuring pO2 in primary aerenchyma, the pO2 was highest in the root base and lower toward the root tip, regardless of the oxygen environment and the age of the root. Regardless of the development of secondary aerenchyma, which is determined by the surface color of the root (dark brown), pO2 in primary aerenchyma near the root base had no significant difference among roots. The decrease of pO2 in primary aerenchyma was observed after injecting nitrogen into the stem portion of 0-3 cm above the water surface. It was confirmed that the primary aerenchyma developed in the adventitious roots seems to be connected to the aerial stem. The oxygen dynamics of primary and secondary aerenchyma were clarified by measuring changes in root pO2 after injecting nitrogen and air into the stem portion of 0-3 cm above the water surface. As a result, the pO2 in the primary aerenchyma decreased and increased when nitrogen and air were injected into the stem. When cortex in the root base was removed, decreased and increased in pO2 was still observed in primary and secondary aerenchyma. Changes in pO2 were observed in nearby primary aerenchyma where the cortex collapse occurred. From these results, it can be seen that primary and secondary aerenchyma function as oxygen transportation pathway, and are connected to each other to transport oxygen.

In chapter 4, To understand the oxygen transfer within S. kunstleri, I clarified the source and pathway of oxygen supplied to adventitious roots. The control of the light condition did not induce a change in root pO2. In other words, oxygen in the adventitious root is fed from atmospheric oxygen rather than oxygen generated from photosynthesis. The removal of secondary aerenchyma from flooded stems induces a decrease in root pO2, which indicates that the secondary aerenchyma developed in stem acts as an oxygen transportation pathway. The entry portion of atmospheric oxygen was determined by measuring the change in pO2 of adventitious roots after injecting nitrogen into the stem portion of 0-3 cm, 3-6 cm, 6-9 cm in height, or leaf. It was confirmed that the stem portion of 0-3 cm above the water surface was the entry portion where atmospheric oxygen was transported from. Three months after the water level was raised by 6 cm above the previous water surface, new adventitious roots developed from the submerged stem near the elevated water surface, and stem portion of 0-3 cm above the elevated water surface was the entry portion of atmospheric oxygen for the newly developed root. The atmospheric oxygen entered from stem portion of 0-3 cm above the elevated water surface did not transported to the previously developed adventitious roots. It has been confirmed that the external oxygen moves from near the previous water surface into the old adventitious roots even after raising the water level. From these results, it was clarified that atmospheric oxygen near the water surface moves to adventitious roots developed from the submerged stem near water surface through the secondary aerenchyma formed in the stem.

The afforestation for destroyed peat swamp forests is becoming more important due to the implementation of Reducing Emissions from Deforestation and Forest Degradation (REDD). Therefore, studies on afforestation technique and appropriate afforestation species for the destructed peat swamp forests are actively being carried out. This study provides the basis for understanding the adaptive mechanism to flooding condition of the tolerant woody plant species, which occurs in the peat swamp forests.

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