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Conocarpus Lancifolius Engl. (Combretaceae) Photosynthetic Apparatus Suffers Damage in Heavy Metal Contaminated Soil

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Conocarpus Lancifolius Engl. (Combretaceae) Photosynthetic Apparatus Suffers Damage in Heavy Metal Contaminated Soil Botany Conocarpus lancifolius Engl. (Combretaceae) photosynthetic apparatus suffers damage in heavy metal contaminated soil Journal: Botany Manuscript ID cjb-2018-0047.R5 Manuscript Type: Article Date Submitted by the 04-Dec-2018 Author: Complete List of Authors: Redha, Amina; Kuwait University, Biological Sciences Al-Hasan, Redha; Kuwait University, Biological Sciences Jose, Jacquilion; Kuwait University, Biological Sciences Saju, Divya; Kuwait University, Biological Sciences Afzal, Mohammad;Draft Kuwait University, Biological Sciences; Retired, Conocarpus lancifolius, chlorophyll fluorescence, electron transport rate, Keyword: photosynthetic rate, photosystem II Is the invited manuscript for consideration in a Special Not applicable (regular submission) Issue? : https://mc06.manuscriptcentral.com/botany-pubs Page 1 of 32 Botany Revised Manuscript ID: cjb-2018-0047.R5 Conocarpus lancifolius Engl. (Combretaceae) photosynthetic apparatus suffers damage in heavy metal contaminated soil Amina Redha, Redah Al-Hasan, Jacquilion Jose, Divya Saju, Mohammad Afzal⌘ Department of Biological Studies, Faculty of Science, Kuwait University, Kuwait Amina Redha: [email protected] Redha Al-Hasan: [email protected] Jacquilion Jose: [email protected] Divya Saju: [email protected] Running title: Conocarpus lancifolius responses to heavy metal stress Corresponding author present address: M. Afzal⌘, 2200-Traemoor Village Way, Nashville, TN 37209, USA. Tel. +1 (352) 681 7347 email: [email protected] 1 https://mc06.manuscriptcentral.com/botany-pubs Botany Page 2 of 32 Abstract Conocarpus lancifolius Engl. (Combretaceae), a heat tolerant plant, could be used for phytoremediation of polluted soil. We aimed to analyze the physiological changes in C. lancifolius exposed to single and mixed heavy metals (HMs), cadmium (Cd2+), nickel (Ni2+), and lead (Pb2+). Under controlled growth conditions, some groups of plants were exposed to a single HM at concentrations of 25 or 50 µM and other groups were exposed to 25 µM HM mixtures, for 30 days. Photosynthetic parameters such as electron transport rate, photosynthetic rate, chlorophyll fluorescence, chlorophyll content index, and photosynthetic pigments were measured. The chloroplast morphology was studied by transmission electron microscopy (TEM). In plants exposed to HM 25 µM, the photosynthetic parameters were unaffected,Draft whereas at HM 50 µM, all parameters significantly decreased until 20 days of exposure followed by an increase until 30 days, indicating a slow adaptability of plants under HM stress. Compared to single HMs, mixed HMs were more toxic at the same concentration. All parameters indicated damage to the photosynthetic apparatus due to stress from mixed HMs at 25 µM and single HMs at 50 µM. TEM analyses showed a dispersion of grana in the chloroplast of the affected C. lancifolius plants. Keywords: Conocarpus lancifolius, chlorophyll fluorescence; electron transport rate; photosynthetic rate; photosystem II 2 https://mc06.manuscriptcentral.com/botany-pubs Page 3 of 32 Botany Introduction Although heavy metals (HMs) are naturally present in the soil, their abundance increases due to industrial activities and oil exploration, causing stress for the proximate animals and plants. Because of the distinct toxicity of HMs, their elevated levels in ecosystems affect the diversity, abundance, and composition of microbial communities, including the micro-flora activities (Baath 1989; Friedlova 2010). Thus, vegetation growing in polluted soil displays growth retardation due to changes in physiological and biochemical parameters (Chibuike and Obiora 2014). The double-membrane-enclosed chloroplast is a sensitive organelle that is most affected by environmental pollutants that enter the cytosol and damage the chloroplast membrane and the photosynthetic apparatus. Factors such as the moisture content of the leaves, theDraft water holding capacity of the soil, and the soil pH, play major roles in determining the levels of HM uptake by the roots, thus affecting the plant’s photosynthetic organelles. Conocarpus lancifolius Engl. (Combretaceae) was introduced into Kuwait from Djibouti where it has thrived in the arid environment and is now widespread. C. lancifolius is also present throughout the Middle East, Southeast Asia, and East Asia, where it is extensively planted along the main boulevards. The plant is seen as an attractive shrub and is therefore purposely planted all over Kuwait and throughout its geographic range. Its conservation, therefore, is important for the people in the region. C. lancifolius is a significant plant with potential applications for health and ecosystem remediation, and therefore, its conservation is of great importance. For instance, Al-Taweel et al. (2016) reported a new ellagic acid derivative from C. lancifolius that shows anti-inflammatory, cytotoxic, and peroxisome proliferator activated 3 https://mc06.manuscriptcentral.com/botany-pubs Botany Page 4 of 32 receptor (PPAR) agonistic activities. Furthermore, Al-Musayeib et al. (2012) demonstrated antiplasmodial, antileishmanial, and antitrypanosomal activities in C. lancifolius, indicating their potential for human health benefits. In terms of ecosystem remediation, Yateem et al. (2008) reported the rhizo-remediation of hydrocarbon- contaminated soil by C. lancifolius and their results suggested that 85.7% of measurable total petroleum hydrocarbon could be degraded in rhizosphere soils associated with C. lancifolius. We initiated a systematic study of C. lancifolius and found that this plant was not only resistant to drought and high salinity, but it could also withstand high desert temperatures and light intensities (Redha et al. 2011, 2012a,b,c, 2013). Currently, there are concerns about the long-term Draftsurvival of C. lancifolius in Kuwait environment, polluted with heavy crude oil. During the Gulf war of 1991, 6-8 million barrels of crude oil were spilled into the marine environment of Kuwait waters, in addition to oil well fires that released massive amounts of soot and toxic gasses into the environment, causing one of the largest man-made environmental disasters in human history. This disaster caused deleterious effects on the local ecosystem due to the persistent toxicity of several HMs and aromatic hydrocarbons, components of crude oil. Along the Wafra road (an oil producing area) the oil-contaminated soil contains Ni at 120.96 mg/kg soil, Pb at 2.9 mg/kg, and Cd at 0.027 mg/kg soil (Kostecki and Behbehani 1995). This can be detrimental to the survival of C. lancifolius, causing public concern. Heavy metal toxicity, caused by free radical generation (Dietz et al. 1999), induces increased synthesis of metal chelating proteins such as phytochelatin, offering a detoxification mechanism to plants for removal of the toxic metal ions and/or a metal 4 https://mc06.manuscriptcentral.com/botany-pubs Page 5 of 32 Botany exchange (Tiecher et al. 2016). Metal stress, however, can damage the plasma membrane (Janicka-Russak et al. 2008) through the formation of free radical and/or binding of metal ions to sulfhydryl groups of membrane proteins and phospholipids, which may cause cellular damage (Devi and Prasad 1999). In plants, this leads to a decline in membrane integrity, undermining cellular transport, energy metabolism, growth, and development (Surowy and Boyer 1991; Binzel 1995; Oufattole et al. 2000). Modification of the plasma membrane, as induced by toxic metals also affects organelle membranes, and results in alterations to the photosynthetic apparatus and consequently energy metabolism (Santos et al. 2014). Heavy metals are highly mobile and are easily transported to the above-ground parts of the plant, principally in plastidsDraft causing ultrastructural modification of the leaf chloroplast. It is known that chloroplasts are the primary targets of metal stress (Solymosi and Bertrand 2012). A damaged chloroplast can impair photosynthesis, transpiration and electron transport rate, photochemical quenching, and photosystem II (PSII) quantum yield. Changes in the thylakoid structures, may cause a reduction in the chlorophyll and carotenoid content, triggering a diminished photosynthetic pigment biosynthesis, and chloroplasts functions (Aggarwal et al. 2011; Cabrita et al. 2016). Changes in the accumulation of polyamines, leading to free, thylakoid- and chromatin-bound polyamines in Pb-exposed barley leaves, have been shown to reduce photosynthetic pigments and photosynthetic parameters in barley leaves (Legocka et al. 2015). As HMs present in crude oil have cumulative negative effects, we carried out this study to assess the effects of HMs on the cultivation of C. lancifolius in soil contaminated with HMs at different concentrations. From the data gathered through this study, we 5 https://mc06.manuscriptcentral.com/botany-pubs Botany Page 6 of 32 report changes in thylakoid ultrastructure of the chloroplasts leading to alterations in photosynthetic activity of C. lancifolius that may be detrimental to its survival in the Kuwaiti environment. Materials and methods Plant materials and growth conditions One hundred and twenty, one-month-old plants with a single shoot with approximately ten leaves, cultivated in plastic pots using peat moss, were obtained from the Public Authority for Agriculture and Fish Resources (PAAFR), a government organization in Kuwait. The pots were transported to Kuwait University, Faculty of Science greenhouse, where they were acclimatized for two weeks. Seventy plants of uniform
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