Ecology

Plant materials, growth conditions and salt treatmentsSoil samples were performed as in previous experiments with S. europaea25, seeds were collected at two maternal sites, the first of which represents natural salinity related to inland salt springs at the health resort of Ciechocinek (Cie) (52°53′N, 18°47′E) characterised by a high soil salinity of ca 100 dS m−1 (~ 1000 mM NaCl), and the second of which is associated with soda factory waste that affects the local environment in Inowrocław-Mątwy (Inw) (52°48′N, 18°15′E) and with a lower salinity of ca 55 dS m−1 (~ 550 mM NaCl). The complete soil description is reported in Piernik et al.51 and Szymanska et al.52,53. Populations are isolated by a distance of ca 40 km without any saline environment between them, however, they were somehow connected due to the presence of salt springs in the nineteenth century. The seeds came from one generation and were collected in early November 2018. The seeds were germinated and grown according to the same steps reported in Cárdenas-Pérez et al.25 with a slight modification in the number of salt treatments at 0, 200, 400, 600, 800 and 1000 mM NaCl. In total, 144 plants were cultivated, and, therefore, a complete randomised factorial design 26 was used, which included (12 plants × 6 treatments × 2 populations) with 14 response variables. After 2 months of development, anatomical analysis such as cell area (A), roundness (R) and maximum cell diameter (Cdiam) were estimated in 12 samples, whereas high and low methyl esterified pectins (HM-HGs and LM-HGs), proline (P), hydrogen peroxide (HP), total soluble protein (Prot), catalase activity (CAT), peroxidase activity (POD), chlorophyll a, b and total (Cha, Chb and TC), carotenoid (Carot) contents, as well as SeNHX1 and SeSOS1 gene expression, were all determined per triplicate (plants were randomly selected). The collection of plant material, comply with relevant institutional, national, and international guidelines and legislation, IUCN Policy Statement on Research Involving Species at Risk of Extinction and Convention on the Trade in Endangered Species of Wild Fauna and Flora. The voucher specimen of the plant material has been deposited in a publicly available herbarium of the Nicolaus Copernicus University in Toruń (Index Herbarium code TRN), deposition number not available (dr. hab. Agnieszka Piernik, prof. NCU undertook the formal identification of plant species, and permission to work with the seeds was provided by the Regional Director of Environmental Protection in Bydgoszcz, WOP.6400.12.2020.JC).Anatomical image analysisFrom the middle primary branch (fleshy segment shoot) of S. europaea plant treatments (0, 200, 400, 600, 800 and 1000 mM NaCl), slices of fresh tissue were obtained by cutting them with a sharp bi-shave blade. The thinner slices of approximately 0.5 mm were selected and used in the microstructure analysis. The size and shape of the stem-cortex cells from the fresh water-storing tissue were characterised by a light microscope (Olympus BX51, USA) connected to a digital camera (DP72 digital microscope camera) and digital acquisition software (DP2-BSW). The microscope images were captured at a magnification of 10 ×/0.30 in RGB scale and stored in TIFF format at 1280 × 1024 pixels. A total of 300 ± 50 cells from five individuals per treatment were analysed. Finally, the shape and size of the cells were obtained from the captured images. Cell image analysis (IA) was performed in ImageJ v. 1.47 (National Institutes of Health, Bethesda, MD, USA). The following anatomical parameters were obtained. Firstly, the cell area (A) was estimated as the number of pixels within the boundary. Secondly, the maximum cell’s diameter (Cdiam) was determined by the distance between the two points separated by the largest coordinates in different orientations, and the cell roundness (R) was obtained through the equation R = (4 A)/(π (Cdiam)2)—where a perfectly round cell has R = 1.0, while elongated cells will show an R → 0. Finally, the degree of succulence (S) in stem was calculated according to24 with slight change S = (Fresh Weight-Dry Weight)/stem Area, where the Area of the stem (As) was calculated as: As = π × r2, the diameter of the stems was obtained according to Cárdenas-Pérez et al.25.Immunolocalisation experimentsThe samples dissected from the middle segment of the shoot (3 individuals per treatment) were prepared for embedding in BMM resin (butyl methacrylate, methyl methacrylate, 0.5% benzoyl ethyl ether (Sigma) with 10 mM DDT (Thermo Fisher Scientific) according to Niedojadło et al.54. Next, specimens were cut on a Leica UCT ultramicrotome into serial semi-thin cross sections (1.5 µm) that were collected on Thermo Scientific Polysine adhesion microscope slides. Before immunocytochemical reaction, the resin was removed with two changes of acetone and washed in distilled water and PBS pH 7.2. After incubation with blocking solution containing 2% BSA (bovine serum albumin, Sigma) in PBS pH 7.2 for 30 min at room temperature, the sections were incubated with anti-pectin rat monoclonal primary antibody JIM7 (recognises partially methylesterified epitopes of homogalacturonan [HG] but does not bind to fully de-esterified HGs) or antibody LM19 (recognises partially methylesterified epitopes of HG and binds strongly to de-esterified HGs) (Plant Probes) diluted 1:50 in 0.2% BSA in PBS pH 7.2 overnight at 4 °C. After washing with PBS pH 7.2, the material was incubated with AlexaFluor 488-conjugated goat anti-rat secondary antibody (Thermo Fisher Scientific) diluted 1:1000 in 0.2% BSA in PBS pH 7.2 for 1 h at 37 °C. Finally, the sections were washed in PBS pH 7.2, dried at room temperature and covered with ProLongTMGold antifade reagent (Thermo Fisher Scientific). The control reactions were performed with the omission of incubation with primary antibodies. Semithin sections were analysed with an Olympus BX50 fluorescence microscope, with an UPlanFI 1009 (N.A. 1.3) oil immersion lens and narrow band filters (U-MNU, U-MNG). The results were recorded with an Olympus XC50 digital colour camera and CellB software (Olympus Soft Imaging Solutions GmbH, Germany).Fluorescence quantitative evaluationFor the quantitative measurement, each experiment was performed using consistent temperatures, incubation times and concentrations of antibodies. The aforementioned ImageJ (1.47v) software was used for image processing and analysis. The fluorescence intensity was measured for five semi-thin sections for each experimental population (Inowrocław and Ciechocinek) at the same magnification (100 ×) and the constant exposure time to ensure comparable results. The threshold fluorescence in the sample was established based on the autofluorescence of the control reaction. The level of signal intensity was expressed in arbitrary units (a.u.) as the mean intensity per μm2 according to Niedojadło et al.54.Biochemical analysisProline content (P) was measured according to Ábrahám et al.55. Five hundred milligrams of fresh stem material was minced on ice and homogenised with 3% aqueous sulfosalicylic acid solution (5 μl mg−1 fresh plant material), centrifuged at 18,000×g, 10 min at 4 °C, and the supernatant was collected. The reaction mixture: 100 μl of 3% sulphosalicylic acid, 200 μl of glacial acetic acid, 200 μl of acidic ninhydrin reagent and 100 μl of supernatant. Acidic ninhydrin reagent was prepared according to Bates et al.56. The standard curve for proline in the concentration range of 0 to 40 μg ml−1. The standard curve equation was y = 0.0467x − 0.0734, R2 = 0.963. P was expressed in mg of proline per gram of fresh weight. Hydrogen peroxide (HP) levels were determined according to the methods described by Velikova et al.57, and 500 mg of stem tissues were homogenised with 5 ml trichloroacetic acid 0.1% (w:v) in an ice bath. The homogenate was centrifuged (12,000×g, 4 °C, 15 min) and 0.5 ml of the supernatant was added to potassium phosphate buffer (0.5 ml) (10 mM, pH 7.0) and 2 ml of 1 M KI. The absorbance was read at 390 nm, and the HP content was given on a standard curve from 0 to 40 mM. The standard curve equation was y = 0.0188x + 0.046, R2 = 0.987. HP concentrations were expressed in nM per gram of fresh weight. Chlorophylls (Cha and Chb) and carotenoids were extracted from fresh plant stems (100 mg) using 80% acetone for 6 h in darkness, and then centrifuged at 10,000 rpm, 10 min. Supernatants were quantified spectrophotometrically. Absorbance was determined at 646, 663 and 470 nm and calculations were performed according to Lichtenthaler and Wellburn58, when 80% of acetone is used as dissolvent. Total chlorophyll content was calculated as the sum of chlorophyll a and b contents.Total CAT activity was determined spectrophotometrically by following the decline in A240 as H2O2 (ε = 39.9 M−1 cm−1) was catabolised, according to the method of Beers and Sizer59. Decrease in absorbance of the reaction at 240 nm was recorded after every 20 s. One unit CAT was defined as an absorbance change of 0.01 units min−1. Total POD activity was determined spectrophotometrically by monitoring the formation of tetraguaiacol (ε = 26.6 mM−1 cm−1) from guaiacol at A470 in the presence of H2O2 by the method of Chance and Maehly60. Increase in absorbance of the reaction solution at 470 nm was recorded after every 20 s. One unit of POD activity was defined as an absorbance change of 0.01 units min−1. Total soluble protein (Prot) content was measured according to Bradford61 using bovine serum albumin (BSA) as a protein standard. Fresh leaf samples (1 g) were homogenised with 4 ml Na-phosphate buffer (pH 7.2) and then centrifuged at 4 °C. Supernatant and dye were pipetted in spectrophotometer cuvettes and absorbances were measured using a UV–vis spectrophotometer (PG instruments T80) at 595 nm62. Prot was determined based on the standard curve y = 1.6565x + 0.0837, R2 = 0.982, for total soluble protein in the concentration range of 0 to 1.2 mg ml−1 BSA. Triplicates per treatment were used for each analysis.Total RNA isolationAfter 2 months of salt treatment, shoots of S. europaea plants (3 individuals per treatment) were washed several times with tap water and then three times with miliQ water. After drying, plant material was frozen in liquid nitrogen, and stored at − 80 °C. Total RNA isolation was performed using RNeasy Plant Mini Kit (Qiagen, Hilden, Germany) according to the manufacturer’s protocol. The quality and quantity of RNA was checked on 1.5% agarose gels in TAE (Tris–HCl, acetic acid, EDTA, pH 8.3) buffer stained with ethidium bromide, and by spectrophotometric measurement (NanoDrop Lite, Thermo Fisher Scientific, Waltham, MA, USA).Cloning of SOS1 gene from S. europaea (SeSOS1)One microgram (1 µg) of total RNA isolated from shoots of S. europaea was primed with 0.5 µg of oligo (dT)20 primer for 5 min at 70 °C. Then 4 µl of ImProm-II 5 × reaction buffer, 2 mM MgCl2, 0.5 mM each dNTP, 20 U of recombinant RNasin ribonuclease inhibitor, and 1 µl of ImProm-II reverse transcriptase (Promega, Madison, WI, USA) were added to a final volume of 20 µl. The reaction was performed at 42 °C for 60 min. To design degenerate primers for SOS1, cDNA sequences from Arabidopsis thaliana (NM_126259.4), Lycopersicon esculentum (AJ717346.1), Mesembryanthemum crystallinum (EF207776.1), Oryza sativa (AY785147.1), Triticum aestivum (AY326952.3), Salicornia brachiata (EU879059.1) were obtained from NCBI GeneBank. The sequences were aligned using the Clustal Omega tool (https://www.ebi.ac.uk/Tools/msa/clustalo/) and three pairs of degenerate primes were designed (listed in Table 4). The PCR reaction mixture includes cDNA, 0.2 µM each primer, 0.2 mM each dNTP, 4 µl of 5 × HF buffer, and 0.5 U of Phusion High-Fidelity DNA polymerase (Thermo Fisher Scientific, Waltham, MA, USA) in a total volume of 20 µl. The thermal conditions were as follows: 98 °C for 30 s, 98 °C for 10 s, gradient between 48 °C and 56 °C for 20 s, 72 °C for 60 s, 32 cycle, final extension for 10 min at 72 °C. A pair of primers deg2_F and deg2_R yielded a PCR product with expected size. The PCR product was purified from agarose gel, cloned into pJET1.2 vector (Thermo Fisher Scientific, Waltham, MA, USA) according to manufacturer’s protocol and sequenced (Genomed, Warsaw, Poland). The obtained partial cDNA sequence was named SeSOS1 and deposited in NCBI GeneBank (acc. no. MZ707082).Table 4 Sequences of the primers used for cloning of SeSOS1 and quantitative real-time PCR.Full size tableReverse transcription reaction and quantitative real-time PCR (qPCR) SeNHX1 and SeSOS1 gene expression analysisPrior to reverse transcription reaction, RNA was treated with DNaseI (Thermo Fisher Scientific, Waltham, MA, USA). The cDNA was synthesised from 1.5 µg of total RNA using a mixture of 2.5 µM oligo(dT)20 primer and 0.2 µg of random hexamers with NG dART RT Kit (Eurx, Gdańsk, Poland) according to the manufacturer’s protocol. The reaction was performed at 25 °C for 10 min, followed by 50 min at 50 °C. The cDNA was stored at − 20 °C.The PCR reaction mixture includes 4 µl of 1/20 diluted cDNA, 0.5 µM gene-specific primers (Table 4) and 5 µl of LightCycler 480 SYBR Green I Master (Roche, Penzberg, Germany) in a total volume of 10 µl. Clathrin adaptor complexes (CAC) was used as a reference gene63. The reaction was performed in triplicate (technical replicates) in LightCycler 480 Instrument II (Roche, Penzberg, Germany). The thermal cycling conditions were as follows: 95 °C for 5 min, 95 °C for 10 s, 60 °C for 20 s, 72 °C for 20 s, 40 cycles. The SYBR Green I fluorescence signal was recorded at the end of the extension step in each cycle. The specificity of the assay was confirmed by the melt curve analysis i.e., increasing the temperature from 55 to 95 °C at a ramp rate 0.11 °C/s. The fold-change in gene expression was calculated using LightCycler 480 Software release 1.5.1.62 (Roche, Penzberg, Germany).Statistical and multivariate analysisIn order to determine the projection of the effect of salt treatment in plants we followed Cárdenas-Pérez et al.25 methodology. A principal component analysis (PCA) was developed using XLSTAT software version 2019.4.165. For this analysis, 14 variables were used, (A, Cdiam, R, Prot, CAT, POD, HM-HGs, LM-HGs, P, HP, Cha, Chb, TC, Carot), arranged in a matrix with the average values obtained from replicates of each treatment and population. A two-way ANOVA comparing treatments within populations and populations within treatments was conducted for all the results with the Holm–Sidak method. The data was fit with a modified three parameter exponential decay using SigmaPlot version 11.066. The relationships between variables were performed using a Pearson analysis, while a significance test (Kaisere Meyere Olkin) was performed in order to determine which variables had a significant correlation with each other (α = 0.05). Then, a 3D plot was developed using the three principal component factors according to the Kaiser criterion which stated that the factors below the unit are irrelevant. The three main factorial scores of the PCA from each sample were used to calculate the distance (D) between the two points (populations) under the same treatment P1 = (x1, y1, z1) and P2 = (x2, y2, z2) in 3D space of the PCA (Eq. 1).$$D ( {P_{1} ,, P_{2} } ) = sqrt {( {x_{2} – x_{1} } )^{2} + ( {y_{2} – y_{1} } )^{2} + ( {z_{2} – z_{1} } )^{2} }$$
(1)
where x, y, and z are the three main factorial scores in the PCA corresponding to the evaluated treatment in Inw and in Cie. Distances were used to evaluate and determine in which salt treatment the greatest differences between the populations were recorded. More

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CAREER Q&A
22 February 2022

Marching in the streets for climate-crisis action

Conservationist Charlie Gardner explains why he joined Scientists for Extinction Rebellion and its civil-disobedience protests.

Christine Ro

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Christine Ro

Christine Ro is a freelance journalist based in Buenos Aires.

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Charlie Gardner speaks at an Extinction Rebellion protest.Credit: Louise Jasper Photography

Conservationist, consultant and activist Charlie Gardner is a lecturer in conservation biology at the Durrell Institute of Conservation and Ecology at the University of Kent in Canterbury, UK. He regularly participates in protests with Scientists for Extinction Rebellion, an offshoot of a broader movement that uses nonviolent civil disobedience to push for action on the climate and biodiversity crises. He has also advised on legislation such as the UK Climate and Ecological Emergency Bill, which seeks to curb UK greenhouse-gas emissions and biodiversity loss, and is currently making its way through Parliament. What drove you to activism? Teaching. Five or six years ago, I was standing in front of a lecture theatre, full of young people who are going to suffer the consequences of climate change much more than I am. I couldn’t stand that I wasn’t doing everything I could. When Extinction Rebellion (XR) was launched in the United Kingdom in October 2018, it felt like the answer. As conservationists, we silently wish that members of the general public cared more about the destruction of nature. Now they are taking to the streets and I have this moral obligation to be there in support.How have you been working with Scientists for XR?In October 2019, a group of scientists came together to create Scientists for XR, which has carried out many actions. These include pasting scientific papers to the walls of the London headquarters of News Corp in 2021 in protest against inadequate climate-change coverage in the company’s newspapers. The group has different functions. One is to provide scientific support for the wider XR movement, so that it remains founded on solid scientific ground. And a second is to advocate. Scientists vocally supporting XR sends a powerful message. Society trusts scientists. A third function is direct action. Scientists for XR groups have been involved in a number of XR events, such as marches and roadblocks. For example, at the 2021 opening of a London Science Museum exhibition sponsored by oil and gas company Shell, some scientists locked themselves to parts of the exhibition in protest against the sponsorship, while our scientist group set up a table outside to demonstrate principles of atmospheric cooling to engage with the public. Events such as this serve to highlight the issue of science museums accepting sponsorship from fossil-fuel companies.How can scientists dip their toes into this type of work?What the public sees of these direct actions is the tip of the iceberg. For every person out on the streets, there are 20 more behind the scenes involved in other tasks: organizing, producing press releases, baking cakes for marchers. Whatever you enjoy doing and have skills in, there is a role for you. Taking part does not have to involve engaging in civil disobedience yourself, or putting yourself in a risky position. One of the most important jobs at a protest is for people to stand at the edges, engaging the public in conversations. That’s a role that scientists can perform fantastically.How have your advocacy and activism benefited you?There’s this crazy notion that scientists shouldn’t speak out because it will damage their reputations. But activism has had the opposite effect on my career. My research is based on conservation in Madagascar; it’s fairly niche. I previously had no global reputation. Since becoming a vocal scientist-activist, my reputation and my visibility as a scientist have soared. Also, activism is great for my mental health. Knowing I’m doing what I can is important to me. There are simply the best people in these movements, and there’s a sense of community. Does being a vocal activist diminish your scientific credibility?Popular perception holds that scientists must be neutral purveyors of information and not speak up about what that information means. Somehow, if we do so, it could damage our credibility.But when scientists take personal risks and make personal sacrifices, that communicates the urgency of the situation in an important way. If scientists are saying that it’s time for action, but not acting themselves, that undermines their own arguments. How do you balance your academic responsibilities with advocacy?For five years, I worked half-time at the University of Kent. I did this deliberately, to allow me the freedom to engage in other activities, including conservation consultancy, activism and writing popular non-fiction. I left that post last year, partly to focus on activism and writing, and partly out of frustration with the precarity of academic life.There are things that enable me to be less single-minded in the pursuit of my career: I come from a position of relative privilege; I’m not interested in accumulating money; and I don’t have children. So I think academia has been a good fit for me, but only because it doesn’t fill my life.

doi: https://doi.org/10.1038/d41586-022-00518-4This interview has been edited for length and clarity.

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CORRESPONDENCE
22 February 2022

Apply Singapore Index on Cities’ Biodiversity at scale

Lena Chan

 ORCID: http://orcid.org/0000-0001-7930-7678

0
,

Kenneth Er

 ORCID: http://orcid.org/0000-0003-4485-7260

1
&

Elizabeth Maruma Mrema

2

Lena Chan

National Parks Board, Singapore Botanic Gardens, Singapore.

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Kenneth Er

National Parks Board, Singapore Botanic Gardens, Singapore.

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Elizabeth Maruma Mrema

Secretariat of the Convention on Biological Diversity, Montreal, Canada.

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In the run-up to the 15th meeting of the Conference of the Parties to the Convention on Biological Diversity, the Singapore Index on Cities’ Biodiversity has been updated to align with the post-2020 global biodiversity framework to halt biodiversity loss (see Nature 601, 298; 2022) and for application at scale (see go.nature.com/3cqrknw).

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Nature 602, 578 (2022)
doi: https://doi.org/10.1038/d41586-022-00476-x

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