An improved, low-cost, hydroponic system for growing Arabidopsis and other plant species under aseptic conditions
- Fulgencio Alatorre-Cobos1, 2,
- Carlos Calderón-Vázquez1, 3,
- Enrique Ibarra-Laclette1, 4,
- Lenin Yong-Villalobos1,
- Claudia-Anahí Pérez-Torres1,
- Araceli Oropeza-Aburto1,
- Alfonso Méndez-Bravo1, 4,
- Sandra-Isabel González-Morales1,
- Dolores Gutiérrez-Alanís1,
- Alejandra Chacón-López1, 5,
- Betsy-Anaid Peña-Ocaña1 and
- Luis Herrera-Estrella1Email author
© Alatorre-Cobos et al.; licensee BioMed Central Ltd. 2014
Received: 15 December 2013
Accepted: 13 March 2014
Published: 21 March 2014
Hydroponics is a plant growth system that provides a more precise control of growth media composition. Several hydroponic systems have been reported for Arabidopsis and other model plants. The ease of system set up, cost of the growth system and flexibility to characterize and harvest plant material are features continually improved in new hydroponic system reported.
We developed a hydroponic culture system for Arabidopsis and other model plants. This low cost, proficient, and novel system is based on recyclable and sterilizable plastic containers, which are readily available from local suppliers. Our system allows a large-scale manipulation of seedlings. It adapts to different growing treatments and has an extended growth window until adult plants are established. The novel seed-holder also facilitates the transfer and harvest of seedlings. Here we report the use of our hydroponic system to analyze transcriptomic responses of Arabidopsis to nutriment availability and plant/pathogen interactions.
The efficiency and functionality of our proposed hydroponic system is demonstrated in nutrient deficiency and pathogenesis experiments. Hydroponically grown Arabidopsis seedlings under long-time inorganic phosphate (Pi) deficiency showed typical changes in root architecture and high expression of marker genes involved in signaling and Pi recycling. Genome-wide transcriptional analysis of gene expression of Arabidopsis roots depleted of Pi by short time periods indicates that genes related to general stress are up-regulated before those specific to Pi signaling and metabolism. Our hydroponic system also proved useful for conducting pathogenesis essays, revealing early transcriptional activation of pathogenesis-related genes.
KeywordsHydroponics Arabidopsis Root Phosphate starvation Pathogenesis
Standardization of growth conditions is an essential factor to obtain high reproducibility and significance in experimental plant biology. While lighting, humidity, and temperature are factors that can be effectively controlled by using plant growth chambers or rooms, media composition can be significantly altered by the physiochemical characteristics and elemental contaminants of different batches of gelling agents [1, 2].
For example, the inventory of changes in root system architecture (RSA) as a plant adaptation to nutrient stress can be influenced by the presence of traces of nutrients in different brands or even batches of agar as reported for the Pi starvation response . Detailed protocols for obtaining real nutrient-deficient solid media for several macro and micronutrients have been recently reported [1, 2]. These protocols describe a careful selection of gelling agents based on a previous chemical characterization that increase the cost and time to set up experiments. In addition those problems associated with media composition, plant growth window is reduced in petri plates (maximum 2–3 weeks) . In vitro culture time can be extended using glass jars but accessibility to the root system is then compromised. Furthermore, additional handling and thus unnecessary plant stress during seedlings transfer to new growth media as well as during plant material collection should be also considered when experiments on solid media are designed.
One strategy for circumventing all problems described above is the use of hydroponic systems for plant culture. Several hydroponic systems have been reported for Arabidopsis [4–13] and some of them are now commercially available (Aeroponics®) . Most of these systems are integrated by a plastic, glass or polycarbonate container with a seed-holder constituted by rock wool, a polyurethane (sponge) piece, a steel or nylon mesh, polyethylene granulate, or a polyvinyl chloride (PVC) piece. Those are open systems, which allow axenic conditions or reduced algal contamination into liquid growth media but sterility is not possible.
Here, we describe step by step a protocol for setting up a simple and low-cost, hydroponic system that allows sterility conditions for growing Arabidopsis and other model plants. This new system is ideal for large-scale manipulation of seedlings and even for fully developed plants. Our system is an improved version of Schlesier et al. , in which the original glass jar and steel seed-holder are substituted by a translucent polypropylene (PE) container and a piece of high-density polyethylene (HDPE) mesh. All components are autoclavable, reusable, cheap, and readily available from local suppliers. The new device designed as seed-holder avoids the use of low-melting agarose as support for seeds, allowing a quick and easy transfer to new media conditions and/or harvest of plant material. The efficiency and functionality of our proposed system is demonstrated and exemplified in experiments that showed typical early transcriptional changes under Pi starvation and pathogen infection.
Results and discussion
Description of the hydroponic system
Comparison between hydroponic systems previously reported and the system proposed here
Agar-filled plastic holder
Rockwool-filled plastic holder
Sponge into a polypropylene sheet
Stainless mesh fixed two metal rigs/Nylon mesh on photo slide mount
Liquid medium container
Magenta GA-7 vessel®
Round-rim glass jars/glass vessel
Intermediate to high
Intermediate to high
Low to intermediate
Reuse of seed-holder
Small to high
Small to intermediate
Small to high
Intermediate to high
Seedling number per holder
Time for moving and sampling large batches of plants between media
Seedling to adult plants
Seedling to adult plants
Protocol for setting up the hydroponic system
Getting a nylon mesh (See Figure 1A)
Get a piece of anti-aphid or anti-insect mesh. Draw a circle (10 cm diameter) using a marker and a cardboard template. Trim the circle using a fork. After tripping the circle, remove color traces on mesh using absolute alcohol. Wash the mesh under running water (Option: Use deionized water). Dry on paper towels. Tip: Use a red color marker for drawing. Red color is easier to clean than other colors.
Making a mesh holder (See Figure 1A,B)
Cut the 500 ml PE container's bottom. Use a scalpel blade. Leave a small edge (0.5 cm width). The mesh circle will put on this edge. For ring A, leave a height of 2.5 cm, for ring B leave 3 cm. Tip: Use a scalpel blade with straight tip to cut easily the container's bottom.
Preparing the container lid
Locate the center of container lid and mark it. Drill the lid center. Seal the small lid hole with a cotton plug. Tip: Use a hot nail to melt a hole in the lid to avoid burrs.
Container and rings and mesh have to be separately sterilized by autoclaving (121°C and 15 psi pressure by 20 minutes). Put container, ring, and mesh groups into poly-bags. For container and rings, close but not seal the poly-bags. If so, pressure variations during sterilization could damage them. Important point: Put the autoclave in liquid media mode. Tip: After sterilization, put poly-bags into another bag for reducing contamination risks.
Hydroponic system assembly (See Figure 1C)
Open the sterilized poly-bags containing containers, rings, meshes, and lids. Put a volume of previously sterilized liquid medium into the container. Tip: the use liquid media at room temperature reduces the steam condensate on container lid and walls. Take a ring B with a dressing tissue forceps and put it into the container just above the liquid media level. Put a mesh piece on the ring B, lift it slowly and then return it on the ring avoiding to form bubbles. Fit the ring A onto the mesh piece. Tip: If it is difficult to fit the ring A onto the mesh piece, warm the ring quickly using a Bunsen burner. Finally, close the container.
Applications of our hydroponic system: 1) Quick transcriptional responses to Pi starvation
Applications of this new hydroponic culture system for model plants were analyzed in this study. Changes during Pi starvation at the transcriptional level associated with the Arabidopsis RSA modifications have been previously described . Here, first we compared the effects of Pi-availability on RSA and the expression profiles of eight marker genes for Pi deficiency in Arabidopsis seedlings grown in hydroponics versus agar media. Then, taking advantage of the short time that is required with this new hydroponic system for transferring plants to different media, early transcriptional responses to Pi depletion were explored at the genome-wide level; such responses have not been previously evaluated.
Arabidopsis growth and Pi-depletion responsive genes on Pi-starved hydroponic media
Although the effects of Pi deficiency on root development were more severe in agar media than in our hydroponic system, the typical root modifications induced by Pi stress (primary root shortening and higher production of lateral roots and root hairs) , were observed in both systems. Differences in the magnitude of RSA alterations in response to Pi-deprivation could be explained by variations in medium composition caused by gelling agents added, and/or the ease to access to Pi available in the growth systems used. It has been previously shown than contaminants such as Pi, iron, and potassium in the gelling compounds can alter the morphophysiological and molecular response to Pi starvation . Hydroponics provides a better control on media composition and allows a direct and homogenous contact of the whole root system with the liquid medium. This condition could be improve nutrient uptake, and under Pi starvation, alleviate the dramatic changes of RSA observed usually in roots of seedlings grown in agar media.
Exploring early genome-wide transcriptional responses to Pi depletion: overview and functional classification of differentially expressed genes
Distribution of functional categories of differentially expressed genes responding to Pi-deprivation under short time points in Arabidopsis roots
Up-/Down-regulated genes** (%)
Time point sampled
Cell cycle and DNA processing
Protein with binding function or cofactor requirement
Regulation of metabolism and protein function
Cell transport, transport facilities, and transport routes
Cellular communication/signal transduction mechanism
Cell rescue, defense and virulence
Interaction with the environment
Systematic interaction with the environment
Biogenesis of cellular components
Early transcriptional responses to low Pi availability involves cell wall modifications, protein activity, oxidation-reduction processes, and hormones-mediated signaling that precede the reported Pi-signaling pathways
According to the functional annotation of the Arabidopsis Information Resource database (TAIR, at http://www.arabidopsis.org), most genes, either induced or repressed during the first 30 min of Pi depletion, are related to cell wall composition, protein activity, oxidation-reduction, and hormones-mediated signaling. Previously known Pi-responsive genes such MGDG SYNTHASE 3 (MGD3), SQDG SYNTHASE 2 (SQD2), PURPLE ACID PHOSPHATASE 22 (PAP22), and S-ADENOSYLMETHIONINE SYNTHASE 1 (SAM1) presented significant changes in expression until the last time point evaluated (2 h). Interestingly, a few transcriptional controllers were expressed differentially throughout the entire experiment.
At 10 minutes, Arabidopsis roots responded to Pi-deprivation with the activation of 27 genes (18.5% of total) involved in polysaccharide degradation, callose deposition, pectin biosynthesis, cell expansion, and microtubule cytoskeleton organization (see group I, Additional file 3). Gene sets related with oxidation-reduction processes, protein activity modifications (ubiquitination, myristoylation, ATP or ion binding), and hormones-mediated signaling (abscisic acid, jasmonic acid) were also represented. Overrepresentation of groups according functional processes was not clear in down-regulated genes, excepting those related to modifications to protein fate (13.5% of total 44 genes).
As Pi depletion progressed (30 min), transcriptional changes related to cell wall decreased while responses to ion transport, signaling by hormones (auxins, abscisic acid, salicylic acid) or kinases were more represented in both induced and repressed genes (Additional file 3). In down-regulated genes, this trend was also found in the last time point (2 h). At 30 minutes, interestingly, genes involved with Pi-homeostasis, e.g. SPX1 and GLYCEROL-3-PHOSPHATE PERMEASE 1 (G3Pp1), were already induced (see group IV and V, Additional file 3).
A higher number of up-regulated genes was found two hours after Pi-depletion. Most induced genes (9 out of 37 genes) were related to ion transport or homeostasis but also to carbohydrate metabolism, oxidation-reduction, signaling, protein activity and development. Importantly, other typical molecular markers for Pi starvation were also induced within 2 hours. Two phosphatidate phosphatases (PAPs) (At3g52820 and At5g44020) were induced gradually according Pi-starvation proceeded. MGD3 and SQD2, both involved with Pi recycling, were also induced at 2 hours (see group VI, Additional file 3). Expression of these genes, together with SPX1 and G3Pp1, indicate that the classical transduction pathways related with Pi-starvation can be triggered as early as two hours after seedlings are exposed to media lacking Pi. SPX1 is strongly induced by Pi starvation and usually classified as member of a system signaling pathway depending of SIZ1/PHR1 reviewed in . Its early induction (3–12 h) has been previously reported  however an “immediate-early response” within few minutes after Pi depletion has been not reported so far. Likewise, a role for an enhanced expression of G3Pp1 inside transduction pathways or metabolic rearrangements triggered by Pi stress is still poorly understood [25, 26]. A recent functional characterization of Arabidopsis glycerophosphodiester phosphodiesterase (GDPD) family suggests glycerol-3-phosphate (G3P) as source of Pi or phosphatidic acid (PA), which could be used by glycerol-3 phosphatase (GPP) or DGDG/SQDG pathways . Early induced expressions of G3Pp1, PAP22, and MGD3 is in agreement with the hypothesis that under Pi deficiency G3P could be first converted into PA by two acyltransferase reactions and Pi would be then released during the subsequent conversion of PA into diacylglycerol (DAG) by PAPs . DAG produced could be incorporated into DGDG or SQDG by MGD2/3 and DGD1/2 and SQD1/2, respectively . MGD2 and MGD3 have been found induced in Arabidopsis seedlings depleted of Pi for 3–12 h . This early transcriptional activity for MGD genes during Pi starvation is also reflected in enhanced enzymatic activities as revealed in Pi-starved bean roots . Increased PA levels and MGDG and DGDG activities have been reported in bean roots starved of Pi for less than 4 h . Early gene expression activation of genes encoding MGDG and DGDG but not PLD/C enzymes suggests G3P and not PC as source for PA and DAG biosynthesis for early Pi signaling and recycling pathways.
According with our data, a specific transduction pathway to Pi deficiency could be preceded by general responses related to stress, which could modify metabolism before triggering specific expression of transcriptional factors. This idea is consistent with previous reports assaying Pi-depletion in Arabidopsis by short and medium-long times (3–48 h), which also reported differentially expressed genes related with pathogenesis, hormone-mediated signaling, protein activity, redox processes, ion transport, and cell wall modifications [25, 28, 34]. Similar results have been recently reported in rice seedlings under Pi starvation for 1 h .
Applications of our hydroponic system: 2) Pathological assays to evaluate systemic defense responses
Here, we describe a practical and inexpensive hydroponic system for growing Arabidopsis and other plants under sterile conditions with an in vitro growth window that goes from seedlings to adult plants. Our system uses recyclable and plastic materials sterilizable by conventional autoclaving that are easy to get at local markets. In contrast to other hydroponic systems previously reported, the components of the system (container size, mesh density, lid) described here can be easily adapted to different experimental designs or plant species. The seed-holder avoids the use of an agarose plug or any other accessory reducing time for setting up experiments and decreasing risks of contamination.
Applications and advantages of our hydroponic system are exemplified in this report. First, rapid transcriptome changes of Arabidopsis roots induced by Pi depletion were detected by a rapid harvest from growth media using our new seed-holder designed. Our analyses confirm that Arabidopsis roots early responses to Pi depletion includes the activation of signaling pathways related to general stress before to trigger those specific to Pi stress, and support the idea that G3P could be a source of Pi and other molecules as PA during early signaling events induced by Pi starvation. Second, our hydroponic system showed a high performance to set up pathogenesis assays.
For solid or liquid media, a 0.1 X Murashige and Skoog (MS) medium, pH 5.7, supplemented with 0.5% sucrose (Sigma-Aldrich), and 3.5 mM MES (Sigma-Aldrich) was used. For solid growth media, agar plant TC micropropagation grade (composition/purity not provided) (A296, Phytotechnology Laboratories, US) from Gelidium species was used at 1% (W/V).
Plant material and growth conditions
Arabidopsis thaliana ecotype Columbia (Col-0, ABRC stock No. 6000 from SALK Institute), marker lines PR1::GUS (At2g14610) (kindly provided by F.M. Ausubel) and AtPT2::GUS (At2g38940) , tobacco cv Xhanti, tomato cv Micro-Tom, and Setaria viridis seeds were used in this study. In all cases, seeds were surface sterilized by sequential treatments with absolute ethanol for 7 min, 20% (v/v) commercial bleach for 7 min and rinsed three times with sterile distilled water. Previous sterilization, Setaria seeds were placed at -80°C overnight as recommended . Arabidopsis sterilized seeds were vernalized at 4°C for 2 days (solid media) or 4 days (hydroponics). For Arabidopsis, 50–65 seeds were directly sowed on the mesh of the seed-holder, and 30–35 seeds in Petri plates (50 ml volume, 15 mm × 150 mm, Phoenix Biomedical). Seedlings of all species evaluated were grown at 22°C, except tobacco which was grown at 28°C, using growth chambers (Percival, Perry, IA, USA) with fluorescent light (100 μmol m-2 s-1) and a photoperiod of 16 h light/8 h dark.
Analysis of root architecture traits
To determine root architecture traits, seedlings were grown on agar plates at an angle of 65° or under hydroponic conditions. Root length was measured from root tip to hypocotyls base. For lateral root (LR) quantification, all clearly visible emerged secondary roots were taken into account when the number of LRs was determined. Root hair density was calculated from root images taken with a digital camera connected to an AFX-II-A stereomicroscope (Nixon, Tokyo). Statistical analysis of quantitative data was performed using the statistical tools (Student’s t test) of Microsoft Excel software.
For histochemical analysis of GUS activity, Arabidopsis seedlings were incubated for 4 h at 37°C in a GUS reaction buffer (0.5 mg ml-1 of 5-bromo-4-chloro-3-indolyl-b-D-glucuronide in 100 mM sodium phosphate buffer, pH 7). Seedlings were cleared using the method previously described . At least 15 transgenic plants were analyzed and imaged using Normarski optics on a Leica DMR microscope.
Roots were collected and immediately frozen and RNA isolated using the Trizol reagent (Invitrogen) and purified with the RNeasy kit (Qiagen) following the manufacturer’s instructions. Spotten glass microarray slides (Arabidopsis Oligonucleotide Array version 3.0) were obtained from University of Arizona (http://.ag.arizona.edu/microarray/). Three biological replicates (150 seedlings per replicate) were used for RNA isolation and two technical replicates (in swap) to the two channel microarrays. Fluorescent labeling of probes, slide hybridization, washing, and image processing was performed as described . A loop design was used in order to contrast the gene expression differences between treatments and time points. Microarray normalization and data analysis to identify differentially expressed genes with at least two-fold change in expression were carried as previously reported .
The microarray data have been deposited in Gene Expression Omnibus (GEO) and are accessible through GEO Series, accession number: GSE53114 (http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE53114).
Total RNA was extracted with Trizol (Invitrogen) and purified using Qiagen RNeasy columns according to the manufacturer’s instructions. cDNA was synthesized using 30 μg of total RNA with SuperScript III Reverse Transcriptase (Invitrogen) and used for qRT-PCR (7500 Real Time PCR System, Applied Biosystems). Expression of marker genes for Pi starvation was analyzed using the oligonucleotides listed in the Additional file 4. Gene expression analyses were performed as previously reported . Briefly, Relative quantification number (RQ) was obtained from the equation (1 + E)2∆∆CT where ∆∆CT represents ∆CT (Treatment)-∆CT (Control) and E is the PCR efficiency. Each CT was previously normalized using the expression levels of ACT2 (At3g18780), PPR (At5g55840), and UPL7 (At3g53090) as internal references.
Bacterial strain P. syringae pv tomato (Pst) DC3000 was cultured on King’s B medium (KB) supplied with 50 μg ml-1 rifampicin. PR1::GUS seedlings were grown hydroponically as described above. For infection of 12 day-old seedlings, a bacterial culture was grown overnight in KB at 28°C. Bacteria were centrifuged, washed three times with sterilized water and resuspended in water to a final OD600 of 0.04. The appropriate volume was added to seedling medium to a final OD600 of 0.002. After infection, plant material was harvested at several time points for GUS histochemical assays and analyzed under a Leica DMR microscope.
This work was partially funded by the Howard Medical Institute (Grant 55003677) to LHE. FAC is indebted to CONACYT for a PhD fellowship (190577). The authors would like to thank R. Sawers (Langebio) for providing S. viridens seeds, J. H. Valenzuela for P. syringae pv tomato strain, J. Antonio Cisneros-Durán (Cinvestav Unidad Irapuato) for his great help with photography and video in this work, and Flor Zamudio-Hernández and María de J. Ortega-Estrada for microarray and qRT-PCR services. We are grateful to the anonymous reviewers for their positive comments and meticulous revision for improving the quality of this manuscript.
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