Elsevier

Aquatic Botany

Volume 142, September 2017, Pages 71-77
Aquatic Botany

Assessment of alcohol dehydrogenase synthesis and aerenchyma formation in the tolerance of Sium L. species (Apiaceae) to water-logging

https://doi.org/10.1016/j.aquabot.2017.07.001Get rights and content

Highlights

  • Aerial-aquatic and terrestrial species of Sium show a similar response to flooding.

  • High plasticity of root systems of the species is regulated by soil moisture.

  • The anaerobic metabolism and aerenchyma formation coexist in the root apices.

  • Anaerobic fermentation is an early systemic response of the plants to root flooding.

  • Adventitious roots include longitudinal and honeycomb-like gas spaces in the cortex.

Abstract

To survive and reproduce under the conditions of limited oxygen supply, plants develop morphological and biochemical features that are either constitutive or induced by flooding. We performed a comparative study of the root cortex structure and alcohol dehydrogenase (ADH) synthesis in widespread aerial-aquatic Sium latifolium and terrestrial S. sisaroideum (Apiaceae) in response to changes in the soil water content to check the hypothesis that plasticity of structural and metabolic traits may ensure survival and adaptation of these species at variable soil moisture − from aerated soil to water-logging. Plant grown under natural and experimental conditions were used for microscopy and enzyme assays. We show that the soil moisture determined changes in the root cortex structure and systemic switching-on of anaerobic fermentation in the investigated species. Water-logging of the terrestrial species S. sisaroideum induced first ADH synthesis and then development of new aerenchymatous adventitious roots that are inherent for aerial-aquatic plants of S. latifolium. Histochemical localization showed high ADH activity in the root apices. The aerenchyma in adventitious roots of both species consisted of longitudinal gas spaces in the inner cortex and enlarged intercellular spaces of a “honeycomb” type in the outer cortex. Thus, both Sium species showed complex anaerobic biochemical and structural responses to flooding, promoting the internal aeration of roots. The high plasticity of the root systems in S. latifolium and S. sisaroideum have led to their widespread distribution in nature.

Introduction

Soil water-logging is an important factor affecting plant growth, development and survival, not only in natural ecosystems but also in agricultural and horticultural systems (Dat et al., 2006, Bailey-Serres and Voesenek, 2008, Parent et al., 2008). Under water-logging, only the root system of a plant is under the anaerobic conditions, while the shoot is under normal atmospheric conditions (Striker, 2012). To survive and reproduce under the conditions of limited oxygen supply, plants develop morphological and biochemical features that are either constitutive or induced by the flooding event (Vartapetian and Jackson, 1997, Dolferus et al., 2000, Visser et al., 2003, Jackson and Colmer, 2005, Benz et al., 2007).

A mechanism of avoiding internal oxygen shortage is the development of aerenchyma, which is a tissue type characterized by prominent intercellular spaces that enhance flooding tolerance in plants by facilitating gas diffusion between the aerial environment and roots (Justin and Armstrong, 1987, Armstrong et al., 1994, Jackson and Armstrong, 1999, Evans, 2003, Aschi-Smiti et al., 2003, Colmer, 2003, Seago et al., 2005, Mano et al., 2006). It is formed in the roots and shoots of wetland species and in some dry-land species in adverse conditions, including high temperature, drought, and nutrient deficiency (Armstrong et al., 1994, Jackson and Armstrong, 1999, Gladish et al., 2006, Haque et al., 2010). Classically, the formation of intercellular spaces is though to be a result of schizogeny and lysigeny during development (Schussler and Longstreth, 2000, Evans, 2003). Schizogeny is the outcome of highly regulated species-specific patterns of cell separation and differential cell expansion creating spaces between cells without cell death occurring. In contrast, lysigenous spaces arise from spatially selective death of grown cortical cells via programmed cell death. Formation of schizogenous aerenchyma is an integral part of normal root development for many wetland species, and it is considered constitutive and pre-adaptive (Seago et al., 2005, Videmšek et al., 2006, Sarkar et al., 2008, Colmer and Voesenek, 2009). In fact, the proportion of aerenchyma is generally considered as a key discriminating factor between wetland and non-wetland plants (Vasellati et al., 2001). Presently, the mechanisms of schizogenous aerenchyma formation are less well understood than the mechanisms of lysigenous aerenchyma formation (Takahashi et al., 2014).

The opposite adaptive strategy is to induce anaerobic fermentation that consists of two steps: carboxylation of pyruvate to acetaldehyde, catalyzed by pyruvate decarboxylase (PDC), and the subsequent reduction of acetaldehyde to ethanol with concomitant oxidation of NAD(P)H to NAD(P)+, catalyzed by alcohol dehydrogenase (ADH) (Vartapetian and Jackson, 1997, Chung and Ferl, 1999, Nakazono et al., 2000, Dat et al., 2004, Parent et al., 2008).

Suitable models to study plant adaptation to changes in soil moisture are aerial-aquatic or amphibious plants that have to adjust not only to oxygen deprivation under flooding, but also to eventual variations of the water level in the basin up to a fully aerated environment (Braendle and Crawford, 1999, Kordyum et al., 2003, Hough-Snee et al., 2015), e.g. species of the genera Alisma, Sagittaria, Sparganium, Persicaria, and Carex. ADH synthesis and aerenchyma development may be used as indicators of plant metabolic and structural adaptation to hypoxic conditions. We have selected two widespread perennial species of the genus Sium (Apiaceae) of different ecology: S. latifolium L. known by the common name “great water-parsnip” and S. sisaroideum DC. known by the common name “skirret“. These closely related species are native throughout Ukraine in the forest and forest-steppe zones. Sium latifolium is usually represented by aerial-aquatic plants growing in wet habitats, such as water meadows and along the shoreline of lakes and rivers; while S. sisaroideum plants are terrestrial. Our long-term phenological observations of these species showed that they are able to sustain well the sudden fluctuations of soil moisture, from flooding to drought during the vegetative period as a result of snowmelt flood, weather changes, or human activity.

Therefore, the main objective of this work was to perform a comparative study of root cortex anatomy and ADH synthesis of both species under field conditions and typical weather conditions. In addition, as S. latifolium aerial-aquatic plants are adapted to root hypoxia, we experimentally investigated the response of terrestrial S. sisaroideum to soil flooding. We expected a high plasticity of the root systems in both species, in which development and functioning are controlled by the soil water content. This would include metabolic adjustment to internal oxygen shortage and structural adaptations directed to avoid oxygen shortage. Our results help to explain the wide distribution of S. latifolium and S. sisaroideum plants in their typical environments and highlight the ecological significance of plant phenotypic plasticity.

Section snippets

Field collection

Sium latifolium and S. sisaroideum are perennial herbaceous plants bearing once-pinnate leaves with toothed leaflets and flowers in terminal and lateral compound umbels. Plants flower from June to August, and the fruiting period lasts from the end of August to the middle of September (Moroziuk and Protopopova, 1986). We studied S. latifolium aerial-aquatic plants growing along the shorelines of the Psjol River near Velyka Bagachka in Poltava region of Ukraine and S. sisaroideum terrestrial

Anatomical traits of the root cortex in aerial-aquatic and terrestrial plants

Root systems of aerial-aquatic S. latifolium and terrestrial S. sisaroideum plants are fibrous and predominantly consists of adventitious roots that originate and develop during the whole vegetation period. Adventitious root primordia are initiated at the hypocotyl near a root collar and in the cotyledonary node. These roots vary in thickness: thin ones, up to 1 mm in diameter, without lateral roots, and thicker ones, to 3–3.5 mm in diameter, with lateral roots. The root system is more vigorous

Discussion

This is the first comparative study of root cortex anatomy and ADH synthesis in aerial-aquatic plants of S. latifolium and terrestrial plants of S. sisaroideum, and it confirmed our hypothesis on the high plasticity of their root systems, especially the root cortex structure, in response to changes in soil water content, lowering due to drop of water level in the river or increasing as a result of long-term abundant raining. When the soil is drying up, the secondary growth of the cortex without

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