Micron-scale phenotyping quantification and three-dimensional microstructure reconstruction of vascular bundles within maize stalks based on micro-CT scanning
Jianjun Du A , Ying Zhang A , Xinyu Guo A , Liming Ma A , Meng Shao A , Xiaodi Pan A and Chunjiang Zhao A B
+ Author Affiliations
- Author Affiliations
A Beijing Key Lab of Digital Plant, Beijing Research Centre for Information Technology in Agriculture, Beijing Academy of Agriculture and Forestry Sciences, No. 11 Shuguang Huayuan Middle Road, Haidian District, Beijing, China.
B Corresponding author. Email: zhaocj@nercita.org.cn
Functional Plant Biology 44(1) 10-22 https://doi.org/10.1071/FP16117
Submitted: 30 March 2016 Accepted: 18 June 2016 Published: 5 August 2016
Abstract
Vascular bundles within maize (Zea mays L.) stalks play a key role in the mechanical support of plant architecture as well as in water and nutrient transportation. Convenient and accurate phenotyping of vascular bundles may help phenotypic identification of germplasm resources for breeding. Based on practical sample preparation procedures for maize stalks, we acquired serials of cross-sectional images using a micro-computed tomography (CT) imaging device. An image processing pipeline dedicated to the phenotyping of vascular bundles was also developed to automatically segment and validate vascular bundles from the cross-sectional images of maize stalks, from which phenotypic traits of vascular bundles, i.e. number, area, and spatial distribution, were calculated. More profound quantification of spatial distribution was given as area ratio of vascular bundles, which described the distribution of vascular bundles associated with the centroid of maize stalks. In addition, three-dimensional visualisation was performed to reveal the spatial configuration and distribution of vascular bundles. The proposed method significantly improves computation accuracy for the phenotypic traits of vascular bundles compared with previous methods, and is expected to be useful for illustrating relationships between phenotypic traits of vascular bundles and their function.
Additional keywords: image segmentation, maize stalk, phenotypic traits.
References
Band LR, Fozard JA, Godin C, Jensen OE, Pridmore T, Bennett MJ, King JR (2012) Multiscale systems analysis of root growth and development: modeling beyond the network and cellular scales. The Plant Cell 24, 3892–3906.| Multiscale systems analysis of root growth and development: modeling beyond the network and cellular scales.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVKls77N&md5=979378ffa3b643b2ad127eef4b587a2fCAS | 23110897PubMed |
Bardage LS (2001) Three-dimensional modeling and visualization of whole Norway spruce latewood tracheids. Wood and Fiber Science 33, 627–638.
Bardage S, Daniel G (2004) Three-dimensional morphological aspects of spruce wood and pulp fibres. In ‘Wood fibre cell walls: methods to study their formation, structure and properties’. pp. 217–229. (Swedish University of Agricultural Sciences: Uppsala, Sweden)
Braun DM, Wang L, Ruan YL (2014) Understanding and manipulating sucrose phloem loading, unloading, metabolism, and signaling to enhance crop yield and food security. Journal of Experimental Botany 65, 1713–1735.
| Understanding and manipulating sucrose phloem loading, unloading, metabolism, and signaling to enhance crop yield and food security.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmtVOlur4%3D&md5=487d4e75e4df1a8ba5a0753ebd0b3476CAS | 24347463PubMed |
Brodersen CR, Roark LC, Pittermann J (2012) The physiological implications of primary xylem organization in two ferns. Plant, Cell & Environment 35, 1898–1911.
| The physiological implications of primary xylem organization in two ferns.Crossref | GoogleScholarGoogle Scholar |
Brodersen CR, Choat B, Chatelet DS, Shackel KA, Matthews MA, McElrone AJ (2013) Xylem vessel relays contribute to radial connectivity in grapevine stems (Vitis vinifera and V. arizonica; Vitaceae). American Journal of Botany 100, 314–321.
| Xylem vessel relays contribute to radial connectivity in grapevine stems (Vitis vinifera and V. arizonica; Vitaceae).Crossref | GoogleScholarGoogle Scholar | 23345417PubMed |
Brooks RA (1977) A quantitative theory of the Hounsfield unit and its application to dual energy scanning. Journal of Computer Assisted Tomography 1, 487–493.
| A quantitative theory of the Hounsfield unit and its application to dual energy scanning.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE1c3hvVOhug%3D%3D&md5=3488ed8ae9a5ca9e8734880af05c82ecCAS | 615229PubMed |
Bucksch A, Burridge J, York LM, Das A, Nord E, Weitz JS, Lynch JP (2014) Image-based high-throughput field phenotyping of crop roots. Plant Physiology 166, 470–486.
| Image-based high-throughput field phenotyping of crop roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvFKrurvP&md5=bad15c8cce50200d33779b4e426257bdCAS | 25187526PubMed |
Choat B, Brodersen CR, McElrone AJ (2015) Synchrotron X-ray microtomography of xylem embolism in Sequoia sempervirens saplings during cycles of drought and recovery. New Phytologist 205, 1095–1105.
| Synchrotron X-ray microtomography of xylem embolism in Sequoia sempervirens saplings during cycles of drought and recovery.Crossref | GoogleScholarGoogle Scholar | 25385085PubMed |
Cloetens P, Mache R, Schlenker M, Lerbs-Mache S (2006) Quantitative phase tomography of Arabidopsis seeds reveals intercellular void network. Proceedings of the National Academy of Sciences of the United States of America 103, 14626–14630.
| Quantitative phase tomography of Arabidopsis seeds reveals intercellular void network.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVOmsb3O&md5=574b98267657b40baf3d39c1a041aa45CAS | 16973748PubMed |
Dorca-Fornell C, Pajor R, Lehmeier C, Pérez-Bueno M, Bauch M, Sloan J, Osborne C, Rolfe S, Sturrock C, Mooney S, Fleming A (2013) Increased leaf mesophyll porosity following transient retinoblastoma-related protein silencing is revealed by microcomputed tomography imaging and leads to a system-level physiological response to the altered cell division pattern. The Plant Journal 76, 914–929.
| Increased leaf mesophyll porosity following transient retinoblastoma-related protein silencing is revealed by microcomputed tomography imaging and leads to a system-level physiological response to the altered cell division pattern.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvV2lsLrN&md5=d7c4dda19e2ea481bd9c7a8dcf107fc9CAS | 24118480PubMed |
Feng HJ, Zhang SP, Ma CJ, Liu P, Dong ST, Zhao B, Zhang JW, Yang JS (2014) Effect of plant density on microstructure of stalk vascular bundles of summer maize (Zea mays L.) and its characteristics of sap flow. Acta Agronomica Sinica 40, 1435–1442.
| Effect of plant density on microstructure of stalk vascular bundles of summer maize (Zea mays L.) and its characteristics of sap flow.Crossref | GoogleScholarGoogle Scholar |
Gong M (1989) Screening methods and indexes of drought resistance in crops and comprehensive evaluation. Journal of Yunnan Agricultural University 4, 73–81.
Hatfield R, Wilson J, Mertens D (1999) Composition of cell walls isolated from cell types of grain sorghum stems. Journal of the Science of Food and Agriculture 79, 891–899.
| Composition of cell walls isolated from cell types of grain sorghum stems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXivVOkt7w%3D&md5=24166ace00ef0636bf95d543f9a7b550CAS |
Heckwolf S, Heckwolf M, Kaeppler SM, de Leon N, Spalding EP (2015) Image analysis of anatomical traits in stalk transections of maize and other grasses. Plant Methods 11, 26
| Image analysis of anatomical traits in stalk transections of maize and other grasses.Crossref | GoogleScholarGoogle Scholar | 25901177PubMed |
Ho QT, Verboven P, Verlinden BE, Schenk A, Delele MA, Rolletschek H, Vercammen J, Nicolaï BM (2010) Genotype effects on internal gas gradients in apple fruit. Journal of Experimental Botany 61, 2745–2755.
| Genotype effects on internal gas gradients in apple fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnsVOgtbY%3D&md5=1046a752257881e5da98295802fdb19bCAS | 20448049PubMed |
Kaminuma E, Yoshizumi T, Wada T, Matsui M, Toyoda T (2008) Quantitative analysis of heterogeneous spatial distribution of Arabidopsis leaf trichomes using micro X-ray computed tomography. The Plant Journal 56, 470–482.
| Quantitative analysis of heterogeneous spatial distribution of Arabidopsis leaf trichomes using micro X-ray computed tomography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVGmtbvP&md5=91186ac767ca3f57d05868c7e76b8d20CAS | 18643999PubMed |
Legland D, Devaux MF, Bouchet B, Guillon F, Lahaye M (2012) Cartography of cell morphology in tomato pericarp at the fruit scale. Journal of Microscopy 247, 78–93.
| Cartography of cell morphology in tomato pericarp at the fruit scale.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlWgsLnE&md5=59490134420c2c3a5a73b7680558e9e5CAS | 22612643PubMed |
Legland D, Devaux MF, Guillon F (2014) Statistical mapping of maize bundle intensity at the stem scale using spatial normalization of replicated images. PLoS One 9, e90673
| Statistical mapping of maize bundle intensity at the stem scale using spatial normalization of replicated images.Crossref | GoogleScholarGoogle Scholar | 24622152PubMed |
Lucas WJ, Groover A, Lichtenberger R, Furuta K, Yadav S-R, Helariutta Y, He X-Q, Fukuda H, Kang J, Brady SM, Patrick JW, Sperry J, Yoshida A, López-Millán A-F, Grusak MA, Kachroo P (2013) The plant vascular system: evolution, development and functions. Journal of Integrative Plant Biology 55, 294–388.
| The plant vascular system: evolution, development and functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnsVajsrk%3D&md5=5c2176817dd3dcf087cd68cf754cdb4cCAS | 23462277PubMed |
Mayo SC, Chen F, Evans R (2010) Micron-scale 3-D imaging of wood and plant microstructure using high-resolution x-ray phase-contrast microtomography. Journal of Structural Biology 171, 182–188.
| Micron-scale 3-D imaging of wood and plant microstructure using high-resolution x-ray phase-contrast microtomography.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3crgtFSqtA%3D%3D&md5=1c529c23a8333e0ff496678e214b3ca3CAS | 20382229PubMed |
McElrone AJ, Choat B, Parkinson DY, MacDowell AA, Brodersen CR (2013) Using high resolution computed tomography to visualize the three dimensional structure and function of plant vasculature. Journal of Visualized Experiments 74, e50162
Mullendore DL, Windt CW, As HV, Knoblauch M (2010) Sieve tube geometry in relation to phloem flow. The Plant Cell 22, 579–593.
| Sieve tube geometry in relation to phloem flow.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmsF2ks74%3D&md5=0fbe13e95738d1b35b85bd067f4fffe2CAS | 20354199PubMed |
Rich SM, Watt M (2013) Soil conditions and cereal root system architecture: review and considerations for linking Darwin and Weaver. Journal of Experimental Botany 64, 1193–1208.
| Soil conditions and cereal root system architecture: review and considerations for linking Darwin and Weaver.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXktFKru7g%3D&md5=f036c4edc42339fda3f1c0c947b0cb32CAS | 23505309PubMed |
Rousseau D, Widiez T, Di Tommaso S, Rositi H, Adrien J, Maire E, Langer M, Olivier C, Peyrin F, Rogowsky P (2015) Fast virtual histology using X-ray in-line phase tomography: application to the 3D anatomy of maize developing seeds. Plant Methods 11, 55
| Fast virtual histology using X-ray in-line phase tomography: application to the 3D anatomy of maize developing seeds.Crossref | GoogleScholarGoogle Scholar | 26688690PubMed |
Shane MW, Mccully ME, Canny MJ (2000) The vascular system of maize stems revisited: implication for water transport and xylem safety. Annals of Botany 86, 245–258.
| The vascular system of maize stems revisited: implication for water transport and xylem safety.Crossref | GoogleScholarGoogle Scholar |
Shi L, Shi T, Broadley MR, White PJ, Long Y, Meng J, Xu F, Hammond JP (2013) High throughput root phenotyping screens identify genetic loci associated with root architectural traits in Brassica napus under contrasting phosphate availabilities. Annals of Botany 112, 381–389.
| High throughput root phenotyping screens identify genetic loci associated with root architectural traits in Brassica napus under contrasting phosphate availabilities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFSitbfI&md5=2a83e012515d2265e0cf5fb999d69f2dCAS | 23172414PubMed |
Staedler YM, Masson D, Schönenberger J (2013) Plant tissues in 3D via x-ray tomography: simple contrasting methods allow high resolution imaging. PLoS One 8, e75295
| Plant tissues in 3D via x-ray tomography: simple contrasting methods allow high resolution imaging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFOntLnF&md5=d20d8adc0b8a4202e0ab2100d4bccf7eCAS | 24086499PubMed |
Tajima K, Chen K-K, Takahashi N, Noda N, Naganatsu Y, Kakigawa H (2009) Three-dimensional finite element modeling from CT images of tooth and its validation. Dental Materials Journal 28, 219–226.
| Three-dimensional finite element modeling from CT images of tooth and its validation.Crossref | GoogleScholarGoogle Scholar | 19496403PubMed |
Torres-Ruiz JM, Jansen S, Choat B, McElrone AJ, Cochard H, Brodribb TJ, Badel E, Burlett R, Bouche PS, Brodersen CR, Li S, Morris H, Delzon S (2015) Direct x-ray microtomography observation confirms the induction of embolism upon xylem cutting under tension. Plant Physiology 167, 40–43.
| Direct x-ray microtomography observation confirms the induction of embolism upon xylem cutting under tension.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXkt1Wmtbs%3D&md5=4fbbfe9131ec5efa35ecb77bce4c9d08CAS | 25378693PubMed |
Truernit E, Bauby H, Dubreucq B, Dubreucq B, Grandjean O, Runion J, Barthélémy J, Palauqui JC (2008) High-resolution whole-mount imaging of three-dimensional tissue organization and gene expression enables the study of phloem development and structure in Arabidopsis. The Plant Cell 20, 1494–1503.
| High-resolution whole-mount imaging of three-dimensional tissue organization and gene expression enables the study of phloem development and structure in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpvVOisLo%3D&md5=6aac8bd7794a500a3042948e453bd055CAS | 18523061PubMed |
Verboven P, Herremans E, Borisjuk L, Helfen L, Ho QT, Tschiersch H, Fuchs J, Nicolaï BM, Rolletschek H (2013) Void space inside the developing seed of Brassica napus and the modelling of its function. New Phytologist 199, 936–947.
| Void space inside the developing seed of Brassica napus and the modelling of its function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1amtLnF&md5=850769dbc7718e20a65771ddf5042a41CAS | 23692271PubMed |
Wilson JR, Mertens DR, Hatfield RD (1993) Isolates of cell types from sorghum stem: digestion, cell wall and anatomical characteristics. Journal of the Science of Food and Agriculture 63, 407–417.
| Isolates of cell types from sorghum stem: digestion, cell wall and anatomical characteristics.Crossref | GoogleScholarGoogle Scholar |
Wu H, Jaeger M, Wang M, Li B, Zhang BG (2011) Three-dimensional distribution of vessels, passage cells and lateral roots along the root axis of winter wheat (Triticum aestivum). Annals of Botany 107, 843–853.
| Three-dimensional distribution of vessels, passage cells and lateral roots along the root axis of winter wheat (Triticum aestivum).Crossref | GoogleScholarGoogle Scholar | 21289027PubMed |
Yan W, Du J, Guo X (2013) Study on segmentation and three-dimensional visualization technology of vascular bundles in cucumber stems. Journal of Agricultural Mechanization Research 2, 9–13.
Zhang Y, Legay S, Barrière Y, Méchin V, Legland D (2013) Color quantification of stained maize stem section describes lignin spatial distribution within the whole stem. Journal of the Science of Food and Agriculture 61, 3186–3192.
| Color quantification of stained maize stem section describes lignin spatial distribution within the whole stem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjsFejsL4%3D&md5=62cd2da1a18fbe7bf30e8bd8efacd1a7CAS |
