The defense system for Bidens pilosa root exudate treatments in Pteris multifida gametophyte

https://doi.org/10.1016/j.ecoenv.2019.01.097Get rights and content

Highlights

  • PCD and AOS are getting a dynamic balance under the exudates treatments.

  • PCD and AOS get increase at first then turn steady under root exudates treatments.

  • Hexadecanoic acid, ethylene glycol and undecane are three major chemicals in root exudates.

  • The activities of SOD, CAT, GR and GST get stronger, and GPX activity turns decrease under the root exudates treatments.

  • The contents of glutathione, Ascorbic acid and reduced ascorbate increased under the root exudates treatments.

Abstract

According to the novel weapons hypothesis, root exudates are the inhibition factors for native species growth and development through invasive plants. It is hypothesized that antioxidant system (AOS) presents an effective role in plant defense system. The allelopathy indexes of P. multifida gametophyte biomass and sporogonium conversions rates turn negative with the dose and time effects, and the synthetical allelopathic effect index was −55.07% at 100% treatments under root exudates treatments. Under transmission electron microscopy, the cell structures turn burry. Next, AOS and programmed cell death (PCD) were tested in this study. In AOS, strong activities of superoxide dismutase, catalase, glutathione reductase and glutathione S-transferase (GST) were identified in gametophyte cells under the treatments, as well as the contents of glutathione, ascorbic acid and reduced ascorbate, while GPX activity decreased. Based on the input (SOD activity) and the output (GST activity) of antioxidant system, and the decreasing system control would be a reason leading gametophyte death under root exudates. At day 10, PCD would get its peak of 46.93% at 100% root exudates. We found a dynamic balance of PCD and AOS under the exudates treatments. We detected hexadecanoic acid, ethylene glycol and undecane are three major chemicals in root exudates. Our results provide a reference of AOS and PCD working under root exudates treatments in plants and offer novel strategy for the native species protection and invasion plants control in environment science.

Introduction

In recent years, with the expansion and increased mobility of humans worldwide, the biodiversity and population of native species has declined (Vitousek et al., 2008). In 2012, according to the preliminary statistics supplied by Ministry of Agriculture of People's Republic of China, the numbers of invasive species were over 448, and the direct economic loss was about 20 billion dollars every year in China. Usually the invasion of plants could produce special chemicals in the soil to inhibit other plants growth and development, and this effect is defined as the allelopathy which is the direct/indirect and harmful effects of one plant as a donor plant on another as a recipient plant through the production of chemical compounds that escape into the environment (Rice, 1984). The evolutionary perspective is generally set in the context of the evolution of increased competitive ability (EICA) that some exotic species reallocate resources from defense to growth, and therefore increase competitiveness (Blossey and Notzold, 1995), and the novel weapons hypothesis (NWH) is defined as some of the inherent competitive advantages of invasive plants are often studied in the context of the negative effects (Bais and Kaushik, 2010). But there are no detailed reports about how plants defense response under the root exudates from the invasion species.

The studies on allelochemicals from root exudates have been an important topic on the invasion plants. For example, the population and germination of native species Plantago lanceolate were inhibited under the phytotoxic effects of root exudates of the invasive plant Heracleum mantegazzianum in Czech Republic (Jandová et al., 2015). Phragmites australis, which is one of the most aggressive invaders and has the potential to suppress neighboring plant species and significant negative effects on germination and growth of Melaleuca ericifolia through the change of pH, electrical conductivity, osmotic potential, phenolics, and dehydrogenase activity by the effects of root exudates (Uddin et al., 2014). Ambrosia artemisiifolia as an invasive plant from North America has threatened most crop production in Europe. In an experiment, growth of tomato was reduced by more than 50% and lettuce root and shoot growth were also inhibited, and the root exudates were phytotoxic to the crops (Vidotto et al., 2013). However, it is still unknown that the defense mechanism working when allelochemicals accumulation in plant cells. In this paper, we not only describe the traditional index of the allelopathy effects, but we would describe the subcellular damage caused in plant cells by root exudates. Furthermore, we try to release the antioxidant system (AOS) working exposed to root exudates, and this problem solving is very important to offer new aspects on how to protect native species in the wild. As we know, gametophyte is a very sensitive plant material to environmental stress (Ong and Ng, 1998, Watkins et al., 2007, Drăghiceanu and Soare, 2016). It was reported that the morphology and chlorophyll fluorescence of 12 kinds fern gametophytes were used to evaluate the desiccation tolerance in tropical areas (Watkins et al., 2007). Pyrrosia pilosellodes (L.) Price gametophyte was used to analyze the dynamic water stress in plant cells (Ong and Ng, 1998). Athyrium filix-femina (L.) Roth and Dryopteris filix-mas (L.) Schott gametophytes were also applied to study cadmium chronic toxicity in plants (Drăghiceanu and Soare, 2016). Therefore, we choose gametophytes to study the physiological response in plants under root exudates treatments.

In previous study, we have described the antioxidants would turn active under the stress of root exudates, resulting in cell damage in gametophyte (Zhang et al., 2016a). Many publications have reported that cell damage has a correlation with increased reactive oxygen species (ROS) (Lesser, 2006, Suzuki et al., 2012). ROS-production accumulating in the chloroplast stroma governs the spread of cell death under the UV irradiation in tobacco leaves (Schraudner et al., 1997). In heavy metal pollution, aluminum-induced oxidative burst through the generation of ROS that lead to cell death and DNA damage in the root cells of Allium cepa (Achary et al., 2012). Meanwhile, when plants treated with the stress of drought, high salinity and freezing, the cell death rates would be enhanced significantly than the control (Xiong and Zhu, 2002). There is no direct evidence about the relationship between cell death and enhanced AOS response developed under root exudates from invasion plants. Thus, we hypothesize that AOS and programmed cell death (PCD) could be major reasons conflicting in plant cell defense under the stress in root exudates. Therefore, the release of the certification would be a great support to NWH and also offer a new aspect on how to control and manage invasion plants.

Section snippets

Root exudate collection

Bidens pilosa is a main invasive plant and it has been reported in more than 22 provinces in middle and south China, and the spread of B. pilosa could reduce agricultural production and change native plant community structures (Hao et al., 2009, Hao et al., 2011). The most of these areas are covered with various kinds of native plants, such as ferns, gymnosperms, angiosperms, etc. The seeds of Bidens pilosa L. were rinsed carefully and thoroughly with distilled water. Subsequently, these seeds

Biomass, spore germination, RI and SE for treatments

Biomass and spore germination of gametophytes exhibited a decreasing trend with increased four gradient concentrations of root exudates (Table 1). The biomass of gametophyte decreased significantly (p <  0.05) under 100% treatment at 7th day, the weight is 32 mg per dish and 46.38% less than the control (69 mg per dish). Meanwhile, the spore germination had the same tendency under the treatment, the germination in treated groups were significantly lower than the control (p < 0.05), especially

The inhibition of root exudate treatments and ultrastructure changes

Usually, the allelopathy could inhibit other plants growing together. For example, a common invasive species, Typha angustifolia, reduced the development and biomass of Bolboschoenus fluviatilis in wetlands in America (Jarchow and Cook, 2009). Invasion species, swine cress, inhibited rice emergence and early seedling growth over 60% and 43% for 10 days in fields (Khaliq et al., 2014). In our study, we found the SE decrease rates were reduced significantly under 100% root exudate treatment than

Conclusion

Under the treatments of Bidens pilosa root exudates, P. multifida gametophyte growth was significantly inhibited as biomass and sporogonium conversions rates were decreased. The gametophyte cell structure was damaged under treatments, chloroplast and mitochondria were deformed and disappeared with increased concentration of root exudates, along with the increased number of osmiophilic granules and dissolved starch granules.

In our study, we identified three allelochemicals as hexadecanoic acid,

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31200233), the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD), Collaborative Innovation Plan of Jiangsu Higher Education, the Jiangsu Government Scholarship for Overseas Studies and the Laboratories of Analytical Biology of the National Museum of Natural History, the Smithsonian Institution.

Author contributions

KZ, YS and YF conceived the study and directed the project. JY performed the TEM test. MX performed the FCM tests and analyses. YS performed the plant physiology experiments. PB and BX participated in manuscript writing and provided suggestions for manuscript improvement. YF, KZ and YS wrote the paper with input from all authors.

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