Dissecting tissue- and species-specific responses of two Plantago species to waterlogging stress at physiological level

Highlights

• Tissue-specific responses to waterlogging stress existed in two Plantgo species.

• The leave of P. fengdouensis were more sensitive to waterlogging stress than that of P. Asiatica.

• The root systems of P. fengdouensis were more tolerant to waterlogging stress than that of P. asiatica.

• The waterlogging tolerance of P. fengdouensis was related to its naturally inhabiting conditions.

Abstract

Plantago fengdouensis is an endangered plant native to islands along the Yangtze River in the Three Gorges Reservoir of China, and P. asiatica is a weed mainly distributed in temperate zone of Asia. Because of contrasting distribution, tissue- and species-specific responses to waterlogging stress of these two accessions were tested in term of changes of reactive oxygen species (ROS) accumulation, membrane lipid peroxidation, free proline, and antioxidant defense systems. Our results suggested that the roots of P. fengdouensis had better tolerance to waterlogging stress than that of P. asiatica, while the leave of P. fengdouensis were more sensitive to waterlogging stress than that of P. asiatica in term of contents of hydrogen peroxide (H₂O₂), superoxide radical (O₂⁻), hydroxyl radical (OH), and malondialdehyde (MDA). The roots of two Plantago species could more efficiently accumulate reduced glutathione (GSH) than leaves under waterlogging conditions. The leaves and roots of P. fengdouensis were more positive responses to waterlogging stress those of P. asiatica in term of GSH. P. fengdouensis were more tolerant to waterlogging stress in term of free proline levels and activities of catalase (CAT), ascorbate peroxidase (APx), and glutathione reductase (GR) than P. asiatica, especially in root systems. The root systems of P. fengdouensis had more tolerant to waterlogging stress than that of P. asiatica, which may be positively related to its natural inhabiting conditions. Our results may be used as indicators of reconstruction of the ex situ populations of the conserved P. fengdouensis.

Introduction

Plantago L. is the largest genus of Plantaginaceae, and comprises about 270 species in the world, and including 20 in China. The aerial parts and seeds of several Plantago species have been widely used as drugs and food due to its considerable bioactivity (Beara et al., 2012, Li et al., 2009, Janković et al., 2012, Nishibe et al., 1995). Plantago asiatica L. (P. asiatica), a weed mainly distributed in temperate zone of Asia, has a wide altitudinal range of habitats, with the highest habitation at 2600 m elevation (Murai et al., 2009). The phytochemical components in P. asiatica have been surveyed by several groups (Nakaoki et al., 1961, Ravn et al., 1990, Nishibe et al., 1995). In contrast, Plantago fengdouensis (Z. E. Zhao & Y. Wang) Y. Wang & Z. Y. Li (P. fengdouensis), an endangered plant native to the Three Gorge Reservoir area of China, was discovered in only two small islands of two counties along the Yangtze River in the Three Gorges Reservoir of China in 2001, and identified and named in 2004 (Wang et al., 2004a, Wang et al., 2004b). Its natural habitat was seasonally flooded due to summer flooding of Yangtze River, and completely and perpetually submerged after the impoundment of the Three Gorges Reservoir (Wang et al., 2007).

Although a large number of Plantago species have been studied for the purpose of phytochemical analysis (Li et al., 2009, Janković et al., 2012, Nishibe et al., 1995, Nishibe, 2002), only few publications addressed the eco-physiological responses of Plantago species to abiotic stress. For example, the altitude variation had different effects on antioxidant system in leaves and in roots of P. major (Ren et al., 1999), and the ozone (O₃) exposure resulted in a reduction in biomass and a decrease in the number of seeds production in P. major (Zheng et al., 2000). Under elevated CO₂ condition, the biomass and total phenolic content of P. maritima increased, while protein content and the maximum carboxylation rate of Rubisco decreased (Davey et al., 2007). P. algarbiensis and P. almogravensis could efficiently accumulate aluminum from soil, especially in root tissues, and aluminum uptake was accompanied by substantial increases of citric, oxalic, malonic and fumaric acids contents in the plantlets of either species (Martins et al., 2013).

Waterlogging often occurs in many parts of the world every year. It often disturbs the plant growth, development, production, and many physiological functions, e.g., inhibition of photosynthesis and accumulation, increases of reactive oxygen species (ROS) production like superoxide radical (O₂⁻), hydrogen peroxide (H₂O₂), and hydroxyl radical (OH), and occurrence of membrane lipid peroxidation (Alhdad et al., 2013, Candan and Tarhan, 2012, Yang et al., 2011). Accordingly, in order to cope with oxidative damages and membrane lipid peroxidation, plants possess a suite of antioxidant enzymatic system and produce some non-enzymatic components like glutathione and free proline to modulate the ROS levels (Alhdad et al., 2013, Candan and Tarhan, 2012, Erkan et al., 2008, Smirnoff and Cumbes, 1989, Yang et al., 2011, Yin et al., 2009c). Perennial plants inhabiting floodplains (or river islands) cannot escape from the flooding conditions and have to endure the occurrences of waterlogging (even flooding) stress. Accordingly, these plants often develop certain phenotypic plasticity and adaptive plasticity to cope with these stresses including adaptive adjustments in biomass allocation and life cycle (Chen and Xie, 2007, Pezeshki, 2001). The present study examined the hypothesis that P. fengdouensis originally inhabiting islands along the Yangtze River was more tolerant to waterlogging stress than P. asiatica widely distributing in Asia, especially in root systems. In addition, we also examined the hypothesis that tissue-specific responses to waterlogging stress between leaves and roots of Plantgo species. These analyses on physiological responses of P. fengdouensis to waterlogging stress may be used as indicators of reconstruction of the ex situ populations of the in situ conserved P. fengdouensis.