Phenotyping roots in darkness: disturbance-free root imaging with near infrared illumination
Rongli Shi A * , Astrid Junker A * , Christiane Seiler A and Thomas Altmann A B
+ Author Affiliations
- Author Affiliations
A Department of Molecular Genetics, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK) Gatersleben, 06466 Seeland, Germany.
B Corresponding author. Email: altmann@ipk-gatersleben.de
Functional Plant Biology 45(4) 400-411 https://doi.org/10.1071/FP17262
Submitted: 31 January 2017 Accepted: 30 October 2017 Published: 5 January 2018
Journal compilation © CSIRO 2018 Open Access CC BY-NC-ND
Abstract
Root systems architecture (RSA) and size properties are essential determinants of plant performance and need to be assessed in high-throughput plant phenotyping platforms. Thus, we tested a concept that involves near-infrared (NIR) imaging of roots growing along surfaces of transparent culture vessels using special long pass filters to block their exposure to visible light. Two setups were used to monitor growth of Arabidopsis, rapeseed, barley and maize roots upon exposure to white light, filter-transmitted radiation or darkness: root growth direction was analysed (1) through short-term cultivation on agar plates, and (2) using soil-filled transparent pots to monitor long-term responses. White light-triggered phototropic responses were detected for Arabidopsis in setup 1, and for rapeseed, barley and maize roots in setups 1 and 2, whereas light effects could be avoided by use of the NIR filter thus confirming its suitability to mimic darkness. NIR image-derived ‘root volume’ values correlated well with root dry weight. The root system fractions visible at the different pot sides and in different zones revealed species- and genotype-dependent variation of spatial root distribution and other RSA traits. Following this validated concept, root imaging setups may be integrated into shoot phenotyping facilities in order to enable root system analysis in the context of whole-plant performance investigations.
Additional keywords: NIR image, NIR pass filter, phototropism, transparent pot.
References
Adu MO, Chatot A, Wiesel L, Bennett MJ, Broadley MR, White PJ, Dupuy LX (2014) A scanner system for high-resolution quantification of variation in root growth dynamics of Brassica rapa genotypes. Journal of Experimental Botany 65, 2039–2048.| A scanner system for high-resolution quantification of variation in root growth dynamics of Brassica rapa genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmsVGktbo%3D&md5=c8b9ba06563b2659148603d2570e11c1CAS |
Cai HG, Chen FJ, Mi GH, Zhang F, Mauren HP, Liu W, Reif JC, Yuan L (2012) Mapping QTLs for root system architecture of maize (Zea mays L.) in the field at different developmental stages. Theoretical and Applied Genetics 125, 1313–1324.
| Mapping QTLs for root system architecture of maize (Zea mays L.) in the field at different developmental stages.Crossref | GoogleScholarGoogle Scholar |
Downie H, Holden N, Otten W, Spiers AJ, Valentine TA, Dupuy LX (2012) Transparent soil for imaging the rhizosphere. PLoS One 7, e44276
| Transparent soil for imaging the rhizosphere.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhtl2jtrzK&md5=e88d3ef3bf6148935f628b03d5d9ffe3CAS |
Fahlgren N, Gehan M, Baxter I (2015) Lights, camera, action, high-throughput plant phenotyping is ready for a close-up. Current Opinion in Plant Biology 24, 93–99.
| Lights, camera, action, high-throughput plant phenotyping is ready for a close-up.Crossref | GoogleScholarGoogle Scholar |
Fiorani F, Schurr U (2013) Future scenarios for plant phenotyping. Annual Review of Plant Biology 64, 267–291.
| Future scenarios for plant phenotyping.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXosFSktLw%3D&md5=1d37eec8f41c1b6d89c9f1fdef18d0fbCAS |
Gioia T, Galinski A, Lenz H, Müller C, Lentz J, Heinz K, Briese C, Putz A, Fiorani F, Watt M, Schurr U, Nagel KA (2017) GrowScreen-PaGe, a non-invasive, high-throughput phenotyping system based on germination paper to quantify crop phenotypic diversity and plasticity of root traits under varying nutrient supply. Functional Plant Biology 44, 76–93.
| GrowScreen-PaGe, a non-invasive, high-throughput phenotyping system based on germination paper to quantify crop phenotypic diversity and plasticity of root traits under varying nutrient supply.Crossref | GoogleScholarGoogle Scholar |
Gruber BD, Giehl RFH, Friedel S, von Wiren N (2013) Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiology 163, 161–179.
| Plasticity of the Arabidopsis root system under nutrient deficiencies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVygsbjM&md5=9c8aed3035d99b34a1e86d24e6b04e9bCAS |
Hubert B, Funke GL (1937) The phototropism of terrestrial roots. Biologisch Jaarboek 4, 286–315.
Iyer-Pascuzzi AS, Symonova O, Mileyko Y, Hao Y, Belcher H, Harer J, Weitz JS, Benfey P (2010) Imaging and analysis platform for automatic phenotyping and trait ranking of plant root systems. Plant Physiology 152, 1148–1157.
| Imaging and analysis platform for automatic phenotyping and trait ranking of plant root systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmsF2ls78%3D&md5=b9e7367dc86ea84bb82c9e66e97717b7CAS |
Junker A, Muraya MM, Weigelt-Fischer K, Arana-Ceballos F, Klukas C, Melchinger AE, Meyer RC, Riewe D, Altmann T (2015) Optimizing experimental procedures for quantitative evaluation of crop plant performance in high throughput phenotyping systems. Frontiers in Plant Science 5, 770
| Optimizing experimental procedures for quantitative evaluation of crop plant performance in high throughput phenotyping systems.Crossref | GoogleScholarGoogle Scholar |
Kiss JZ, Miller KM, Ogden LA, Roth KK (2002) Phototropism and gravitropism in lateral roots of Arabidopsis. Plant & Cell Physiology 43, 35–43.
| Phototropism and gravitropism in lateral roots of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtVyqtrk%3D&md5=db776e1ba641db4e6e9376a1dc9d43f6CAS |
Kiss JZ, Mullen JL, Correll MJ, Hangarter RP (2003a) Phytochromes A and B mediate red-light-induced positive phototropism in roots. Plant Physiology 131, 1411–1417.
| Phytochromes A and B mediate red-light-induced positive phototropism in roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXisFelsLw%3D&md5=3105c4bb3f2b365ba2dfaa23495ede3fCAS |
Kiss JZ, Correll MJ, Mullen JL, Hangarter RP, Edelmann RE (2003b) Root phototropism, how light and gravity interact in shaping plant form. Gravitational and Space Biology Bulletin 16, 55–60.
Kumar B, Abdel-Ghani AH, Reyes-Matamoros J, Hochholdinger F, Lübberstedt T (2012) Genotypic variation for root architecture traits in seedlings of maize (Zea mays L.) inbred lines. Plant Breeding 131, 465–478.
| Genotypic variation for root architecture traits in seedlings of maize (Zea mays L.) inbred lines.Crossref | GoogleScholarGoogle Scholar |
Kutschera U, Briggs WR (2012) Root phototropism, from dogma to the mechanism of blue light perception. Planta 235, 443–452.
| Root phototropism, from dogma to the mechanism of blue light perception.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XivFKqtL8%3D&md5=318267447a68c16aa9247830a369317fCAS |
Lee HJ, Park YJ, Ha JH, Baldwin IT, Park CM (2017) Multiple routes of light signaling during root photomorphogenesis. Trends in Plant Science 22, 803–812.
| Multiple routes of light signaling during root photomorphogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhtFSmt7vF&md5=1f8c800b37ca90a05afac24a3a57d1a3CAS |
Li J, Li G, Wang H, Deng XW (2011) Phytochrome signaling mechanisms. In ‘The Arabidopsis book’. (American Society of Plant Biologists: Washington, DC, USA).
Liscum E, Askinosie SK, Leuchtman DL, Morrow J, Willenburg KT, Coats DR (2014) Phototropism: growing towards an understanding of plant movement. The Plant Cell 26, 38–55.
| Phototropism: growing towards an understanding of plant movement.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXks1Sgtb8%3D&md5=430cd979c6d0242eb34bd458d2b1dde8CAS |
Lobet G, Pages L, Draye X (2011) A novel image analysis toolbox enabling quantitative analysis of root system architecture. Plant Physiology 157, 29–39.
| A novel image analysis toolbox enabling quantitative analysis of root system architecture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1Sit77P&md5=02c0ce015aff0db10c034265a812493bCAS |
Mairhofer S, Sturrock C, Wells DM, Bennett MJ, Moonery SJ, Pridmore T (2015) On the evaluation of methods for the recovery of plant root systems from X-ray computed tomography images. Functional Plant Biology 42, 460–470.
| On the evaluation of methods for the recovery of plant root systems from X-ray computed tomography images.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXms1OjsLw%3D&md5=e3cd6f6362551428d0c9f7cca05f589bCAS |
Muraya MM, Chu J, Zhao Y, Junker A, Klukas C, Reif JC, Altmann T (2016) Genetic variation of growth dynamics in maize (Zea mays L.) revealed through automated non-invasive phenotyping. The Plant Journal 89, 366–380.
| Genetic variation of growth dynamics in maize (Zea mays L.) revealed through automated non-invasive phenotyping.Crossref | GoogleScholarGoogle Scholar |
Nagel KA, Kastenholz B, Jahnke S, van Dusschoten D, Aach T, Mühlich M, Truhn D, Scharr H, Terjung S, Walter A, Schurr U (2009) Temperature responses of roots, impact on growth, root system architecture and implications for phenotyping. Functional Plant Biology 36, 947–959.
| Temperature responses of roots, impact on growth, root system architecture and implications for phenotyping.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlOgs7vM&md5=e11622e5a5708baf3ecc3b21c086e1deCAS |
Nagel KA, Putz A, Gilmer F, Heinz K, Fischbach A, Pfeifer J, Faget M, Blossfeld S, Ernst M, Dimaki C, Kastenholz B, Kleinert AK, Galinski A, Scharr H, Fiorani F, Schurr U (2012) GROWSCREEN-Rhizo is a novel phenotyping robot enabling simultaneous measurements of root and shoot growth for plants grown in soil-filled rhizotrons. Functional Plant Biology 39, 891–904.
| GROWSCREEN-Rhizo is a novel phenotyping robot enabling simultaneous measurements of root and shoot growth for plants grown in soil-filled rhizotrons.Crossref | GoogleScholarGoogle Scholar |
Pace J, Gardner C, Romay C, Ganapathysubramanian B, Lübberstedt T (2015) Genome-wide association analysis of seedling root development in maize (Zea mays L.). BMC Genomics 16, 47
| Genome-wide association analysis of seedling root development in maize (Zea mays L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXkt1Wns78%3D&md5=6de82675ddf2b71114170b5005419c76CAS |
Pacheco-Villalobos D, Hardtke CS (2012) Natural genetic variation of root system architecture from Arabidopsis to Brachypodium, towards adaptive value. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 367, 1552–1558.
| Natural genetic variation of root system architecture from Arabidopsis to Brachypodium, towards adaptive value.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xos1Oqs74%3D&md5=5b45e3224ad49e83a45234a5156f59f0CAS |
Pestsova E, Lichtblau D, Wever C, Presterl T, Bolduan T, Ouzunova M, Westhoff P (2016) QTL mapping of seedling root traits associated with nitrogen and water use efficiency in maize. Euphytica 209, 585–602.
| QTL mapping of seedling root traits associated with nitrogen and water use efficiency in maize.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhvFSiug%3D%3D&md5=743a0b0ad7cb3de71d5d398f4f35146dCAS |
Rao IM, Miles JW, Beebe SE, Horst WJ (2016) Root adaptations to soils with low fertility and aluminium toxicity. Annals of Botany 118, 593–605.
| Root adaptations to soils with low fertility and aluminium toxicity.Crossref | GoogleScholarGoogle Scholar |
Ruppel NJ, Hangarter RP, Kiss JZ (2001) Red-light-induced positive phototropism in Arabidopsis roots. Planta 212, 424–430.
| Red-light-induced positive phototropism in Arabidopsis roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtV2kt78%3D&md5=16aae60b74df0575890e1f6a41b36647CAS |
Ruts T, Matsubara S, Walter A (2013) Synchronous high-resolution phenotyping of leaf and root growth in Nicotiana tabacum over 24-h periods with GROWMAP-plant. Plant Methods 9, 2
| Synchronous high-resolution phenotyping of leaf and root growth in Nicotiana tabacum over 24-h periods with GROWMAP-plant.Crossref | GoogleScholarGoogle Scholar |
Saengwilai P, Tian X, Lynch JP (2014) Low crown root number enhances nitrogen acquisition from low-nitrogen soils in maize. Plant Physiology 166, 581–589.
| Low crown root number enhances nitrogen acquisition from low-nitrogen soils in maize.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvFKit7rF&md5=9c62321700e2ffe5ccb678f85001ba54CAS |
Schmittgen S, Metzner R, Van Dusschoten D, Jansen M, Fiorani F, Jahnke S, Rascher U, Schurr U (2015) Magnetic resonance imaging of sugar beet taproots in soil reveals growth reduction and morphological changes during foliar Cercospora beticola infestation. Journal of Experimental Botany 66, 5543–5553.
| Magnetic resonance imaging of sugar beet taproots in soil reveals growth reduction and morphological changes during foliar Cercospora beticola infestation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitVOitbbE&md5=6efb5ec12f7024d93ef57c7f1d60367bCAS |
Shrestha R, Al-Shugeairy Z, Al-Ogaidi F, Munasinghe M, Radermacher M, Vandenhirtz J, Price AH (2014) Comparing simple root phenotyping methods on a core set of rice genotypes. Plant Biology 16, 632–642.
| Comparing simple root phenotyping methods on a core set of rice genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmtV2msrY%3D&md5=96871ff2303d90f7ffc29245429f6a83CAS |
Silva-Navas J, Moreno-Risueno MA, Manzano C, Pallero-Baena M, Navarro-Neila S, Tellez-Robledo B, Garcia-Mina J, Baigorri R, Gallego J, del Pozo JC (2015) D-Root, a system for cultivating plants with the roots in darkness or under different light conditions. The Plant Journal 84, 244–255.
| D-Root, a system for cultivating plants with the roots in darkness or under different light conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsFygtL3O&md5=579da6925bd3df4c0fa5d2ff664d0262CAS |
Trachsel S, Kaeppler SM, Brown KM, Lynch JP (2011) Shovelomics: high throughput phenotyping of maize (Zea mays L.) root architecture in the field. Plant and Soil 341, 75–87.
| Shovelomics: high throughput phenotyping of maize (Zea mays L.) root architecture in the field.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjt1Wjsrc%3D&md5=0e42dd86d59caa3c57f5abef42de836fCAS |
Uga Y, Ebana K, Abe J, Morita S, Okuno K, Yano M (2009) Variation in root morphology and anatomy among accessions of cultivated rice (Oryza sativa L.) with different genetic backgrounds. Breeding Science 59, 87–93.
| Variation in root morphology and anatomy among accessions of cultivated rice (Oryza sativa L.) with different genetic backgrounds.Crossref | GoogleScholarGoogle Scholar |
Uga Y, Sugimoto K, Ogawa S, Rane J, Ishitani M, Hara N, Kitomi Y, Inukai Y, Ono K, Kanno N, Inoue H, Takehisa H, Motoyama R, Nagamura Y, Wu J, Matsumoto T, Takai T, Okuno K, Yano M (2013) Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nature Genetics 45, 1097–1102.
| Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1WgsrnM&md5=b88478ee447eccd55130d1b472ac11a6CAS |
Wang YX, Wang Z, Suo B, Gu YJ, Wang HH, Chen YH, Dai YX (2007) Discussion on photoreceptor for negative phototropism in rice roots. Rice Science 14, 315–318.
| Discussion on photoreceptor for negative phototropism in rice roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkvVegug%3D%3D&md5=bc0ba86f501c142e404f41456e10a899CAS |
Wells DM, French AP, Naeem A, Ishaq O, Traini R, Hijazi H, Bennett MJ, Pridmore TP (2012) Recovering the dynamics of root growth and development using novel image acquisition and analysis methods. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 367, 1517–1524.
| Recovering the dynamics of root growth and development using novel image acquisition and analysis methods.Crossref | GoogleScholarGoogle Scholar |
White PJ, George T, Gregory PJ, Bengough AG, Hallett PD, Mckenzie M (2013) Matching roots to their environment. Annals of Botany 112, 207–222.
| Matching roots to their environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFSiur7P&md5=392383aff4a41a9e44817807253f5c72CAS |
Xu W, Ding G, Yokawa K, Baluska F, Li Q, Liu Y, Shi W, Liang J, Zhang J (2013) An improved agar-plate method for studying root growth and response of Arabidopsis thaliana. Scientific Reports 3, 1273
| An improved agar-plate method for studying root growth and response of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
