Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH FRONT

Non-invasive approaches for phenotyping of enhanced performance traits in bean

Uwe Rascher A D , Stephan Blossfeld A , Fabio Fiorani A , Siegfried Jahnke A , Marcus Jansen A , Arnd J. Kuhn A , Shizue Matsubara A , Lea L. A. Märtin A , Andrew Merchant B , Ralf Metzner A , Mark Müller-Linow A , Kerstin A. Nagel A , Roland Pieruschka A , Francisco Pinto A , Christina M. Schreiber A , Vicky M. Temperton A , Michael R. Thorpe A , Dagmar van Dusschoten A , Elizabeth van Volkenburgh C , Carel W. Windt A and Ulrich Schurr A
+ Author Affiliations
- Author Affiliations

A Institute of Bio- and Geosciences, IBG-2: Plant Sciences, Forschungszentrum Jülich GmbH, Leo-Brandt-Str., 52425 Jülich, Germany.

B Faculty of Agriculture, Food and Natural Resources, Biomedical Building, The University of Sydney, 1 Central Avenue, Eveleigh, NSW 2006, Australia.

C Biology Department, Box 35-5325, University of Washington, Seattle, WA 98195, USA.

D Corresponding author. Email: u.rascher@fz-juelich.de

Functional Plant Biology 38(12) 968-983 https://doi.org/10.1071/FP11164
Submitted: 26 July 2011  Accepted: 15 October 2011   Published: 1 December 2011

Abstract

Plant phenotyping is an emerging discipline in plant biology. Quantitative measurements of functional and structural traits help to better understand gene–environment interactions and support breeding for improved resource use efficiency of important crops such as bean (Phaseolus vulgaris L.). Here we provide an overview of state-of-the-art phenotyping approaches addressing three aspects of resource use efficiency in plants: belowground roots, aboveground shoots and transport/allocation processes. We demonstrate the capacity of high-precision methods to measure plant function or structural traits non-invasively, stating examples wherever possible. Ideally, high-precision methods are complemented by fast and high-throughput technologies. High-throughput phenotyping can be applied in the laboratory using automated data acquisition, as well as in the field, where imaging spectroscopy opens a new path to understand plant function non-invasively. For example, we demonstrate how magnetic resonance imaging (MRI) can resolve root structure and separate root systems under resource competition, how automated fluorescence imaging (PAM fluorometry) in combination with automated shape detection allows for high-throughput screening of photosynthetic traits and how imaging spectrometers can be used to quantify pigment concentration, sun-induced fluorescence and potentially photosynthetic quantum yield. We propose that these phenotyping techniques, combined with mechanistic knowledge on plant structure–function relationships, will open new research directions in whole-plant ecophysiology and may assist breeding for varieties with enhanced resource use efficiency varieties.

Additional keywords: fluorescence, imaging spectroscopy, non-invasive, resource use efficiency.


References

Ainsworth EA, Yendrek CR, Skoneczka JA, Long SP (2011) Accelerating yield potential in soybean: potential targets for biotechnological improvement. Plant, Cell & Environment
Accelerating yield potential in soybean: potential targets for biotechnological improvement.Crossref | GoogleScholarGoogle Scholar |

Alonso L, Gomez-Chova L, Vila-Frances J, Amoros-Lopez J, Guanter L, Calpe J, Moreno J (2008) Improved Fraunhofer line discrimination method for vegetation fluorescence quantification. IEEE Geoscience and Remote Sensing Letters 5, 620–624.
Improved Fraunhofer line discrimination method for vegetation fluorescence quantification.Crossref | GoogleScholarGoogle Scholar |

Ananyev G, Kolber ZS, Klimov D, Falkowski PG, Berry JA, Rascher U, Martin R, Osmond CB (2005) Remote sensing of heterogeneity in photosynthetic efficiency, electron transport and dissipation of excess light in Populus deltoides stands under ambient and elevated CO2 concentrations, and in a tropical forest canopy, using a new laser-induced fluorescence transient device. Global Change Biology 11, 1195–1206.
Remote sensing of heterogeneity in photosynthetic efficiency, electron transport and dissipation of excess light in Populus deltoides stands under ambient and elevated CO2 concentrations, and in a tropical forest canopy, using a new laser-induced fluorescence transient device.Crossref | GoogleScholarGoogle Scholar |

Armengaud P, Zambaux K, Hills A, Sulpice R, Pattison RJ, Blatt MR, Amtmann A (2009) EZ-Rhizo: integrated software for the fast and accurate measurement of root system architecture. The Plant Journal 57, 945–956.
EZ-Rhizo: integrated software for the fast and accurate measurement of root system architecture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjslSltr0%3D&md5=8793380f6a2fdd3c8ac709de57e00c2cCAS |

Asner GP, Vitousek PM (2005) Remote analysis of biological invasion and biogeochemical change. Proceedings of the National Academy of Sciences of the United States of America 102, 4383–4386.
Remote analysis of biological invasion and biogeochemical change.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXivFCrtbs%3D&md5=b97b395f9ee5b241c0025f01a4f82a6bCAS |

Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annual Review of Plant Biology 59, 89–113.
Chlorophyll fluorescence: a probe of photosynthesis in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqsL8%3D&md5=cb401be9e3802e2a6dd7d60ad3a2e810CAS |

Bezemer TM, Fountain MT, Barea JM, Christensen S, Dekker SC, Duyts H, van Hal R, Harvey JA, Hedlund K, Maraun M, Mikola J, Mladenov AG, Robin C, de Ruiter PC, Scheu S, Setälä H, Šmilauer P, van der Putten WH (2010) Divergent composition but similar function of soil food webs beneath individual plants: plant species and community effects. Ecology 91, 3027–3036.
Divergent composition but similar function of soil food webs beneath individual plants: plant species and community effects.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cblslSmtQ%3D%3D&md5=ae2cb5c68489a6c61c9b6ee1e9605a66CAS |

Biskup B, Scharr H, Schurr U, Rascher U (2007) A stereo imaging system for measuring structural parameters of plant canopies. Plant, Cell & Environment 30, 1299–1308.
A stereo imaging system for measuring structural parameters of plant canopies.Crossref | GoogleScholarGoogle Scholar |

Biskup B, Scharr H, Fischbach A, Wiese-Klinkenberg A, Schurr U, Walter A (2009) Diel growth cycle of isolated leaf discs analyzed with a novel, high-throughput three-dimensional imaging method is identical to that of intact leaves. Plant Physiology 149, 1452–1461.
Diel growth cycle of isolated leaf discs analyzed with a novel, high-throughput three-dimensional imaging method is identical to that of intact leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsFCiur0%3D&md5=5388dd2d6485a45351e50f9a2a62816cCAS |

Bottomley PA, Rogers HH, Foster TH (1986) NMR imaging shows water distribution and transport in plant roof systems in situ. Proceedings of the National Academy of Sciences of the United States of America 83, 87–89.
NMR imaging shows water distribution and transport in plant roof systems in situ.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnivFamuw%3D%3D&md5=7409e71df21b151a12b225189f5ac289CAS |

Bouguet JY (2005) Camera calibration toolbox for Matlab. Available at http://www.vision.caltech.edu/bouguetj/calib_doc/ [Verified 28 October 2011]

Brown RJS, Chandler R, Jackson JA, Kleinberg RL, Miller MN, Paltiel Z, Prammer MG (2001) The history of NMR well logging. Concepts of Magnetic Resoncance 13, 335–413.

Brown MZ, Burschka D, Hager GD (2003) Advances in computational stereo. IEEE Transactions on Pattern Analysis and Machine Intelligence 25, 993–1008.
Advances in computational stereo.Crossref | GoogleScholarGoogle Scholar |

Bühler J, Huber G, Schmid F, Blümler P (2011) Analytical model for long-distance tracer-transport in plants. Journal of Theoretical Biology 270, 70–79.
Analytical model for long-distance tracer-transport in plants.Crossref | GoogleScholarGoogle Scholar |

Curran PJ (1989) Remote-sensing of foliar chemistry. Remote Sensing of Environment 30, 271–278.
Remote-sensing of foliar chemistry.Crossref | GoogleScholarGoogle Scholar |

Damm A, Elbers J, Erler E, Gioli B, Hamdi K, Hutjes R, Kosvancova M, Meroni M, Miglietta F, Moersch A, Moreno J, Schickling A, Sonnenschein R, Udelhoven T, van der Linden S, Hostert P, Rascher U (2010) Remote sensing of sun induced fluorescence to improve modeling of diurnal courses of gross primary production (GPP). Global Change Biology 16, 171–186.
Remote sensing of sun induced fluorescence to improve modeling of diurnal courses of gross primary production (GPP).Crossref | GoogleScholarGoogle Scholar |

de Kroon H (2007) How do roots interact? Science 318, 1562–1563.
How do roots interact?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVemtLjL&md5=f6ae159fd380cfc363a003abbbf3cc21CAS |

Dermody O, Long SP, McConnaughay K, Delucia EH (2008) How do elevated CO2 and O3 affect the interception and utilization of radiation by a soybean canopy? Global Change Biology 14, 556–564.
How do elevated CO2 and O3 affect the interception and utilization of radiation by a soybean canopy?Crossref | GoogleScholarGoogle Scholar |

Duvick DN (2005) The contribution of breeding to yield advances in maize (Zea mays L.). Advances in Agronomy 86, 83–145.
The contribution of breeding to yield advances in maize (Zea mays L.).Crossref | GoogleScholarGoogle Scholar |

Ehleringer JR, Forseth IN (1980) Solar tracking by plants. Science 210, 1094–1098.
Solar tracking by plants.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cvlsVegtg%3D%3D&md5=573f01e3407fe9447cb37b36215a2e93CAS |

Evans LT (1997) Adapting and improving crops: the endless task. Philosophical Transactions of the Royal Society B. Biological Sciences 352, 901–906.
Adapting and improving crops: the endless task.Crossref | GoogleScholarGoogle Scholar |

Felzenszwalb PF, Huttenlocher D (1998) Image segmentation using local variation. In ‘Proceedings of IEEE Conference on Computer Vision and Pattern Recognition’. pp. 98–104. (IEEE Computer Society: Washington, DC)

Flexas J, Briantais JM, Cerovic Z, Medrano H, Moya I (2000) Steady-state and maximum chlorophyll fluorescence responses to water stress in grapevine leaves: a new remote sensing system. Remote Sensing of Environment 73, 283–297.
Steady-state and maximum chlorophyll fluorescence responses to water stress in grapevine leaves: a new remote sensing system.Crossref | GoogleScholarGoogle Scholar |

Frak E, Le Roux X, Millard P, Adam B, Dreyer E, Escuit C, Sinoquet H, Vandame M, Varlet-Grancher C (2002) Spatial distribution of leaf nitrogen and photosynthetic capacity within the foliage of individual trees: disentangling the effects of local light quality, leaf irradiance, and transpiration. Journal of Experimental Botany 53, 2207–2216.
Spatial distribution of leaf nitrogen and photosynthetic capacity within the foliage of individual trees: disentangling the effects of local light quality, leaf irradiance, and transpiration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xpt1Kgtb4%3D&md5=3ec148e91b1f9c8911473dcac5be1f3dCAS |

Franke J, Menz G, Oerke EC, Rascher U (2005) Comparison of multi- and hyperspectral imaging data of leaf rust infected wheat plants. In ‘Remote Sensing for Agriculture, Ecosystems, and Hydrology VII. Proceedings of SPIE Vol. 5976’. (Eds M Owe, G D’Urso) pp. 341–350. (SPIE Press: Brugge, Belgium)

Fua P (1993) A parallel stereo algorithm that produces dense depth maps and preserves image features. Machine Vision and Applications 6, 35–49.
A parallel stereo algorithm that produces dense depth maps and preserves image features.Crossref | GoogleScholarGoogle Scholar |

Gamon JA, Penuelas J, Field CB (1992) A narrow-waveband spectral index that tracks diurnal changes in photosynthetic efficiency. Remote Sensing of Environment 41, 35–44.
A narrow-waveband spectral index that tracks diurnal changes in photosynthetic efficiency.Crossref | GoogleScholarGoogle Scholar |

Gilbert ME, Zwieniecki MA, Holbrook NM (2011) Independent variation in photosynthetic capacity and stomatal conductance leads to differences in intrinsic water use efficiency in 11 soybean genotypes before and during mild drought. Journal of Experimental Botany 62, 2875–2887.
Independent variation in photosynthetic capacity and stomatal conductance leads to differences in intrinsic water use efficiency in 11 soybean genotypes before and during mild drought.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmsVyksbY%3D&md5=3d27b99c5f6c3e39017af035f98dae28CAS |

Gitelson AA, Merzlyak MN, Chivkunova OB (2001) Optical properties and nondestructive estimation of anthocyanin content in plant leaves. Photochemistry and Photobiology 74, 38–45.
Optical properties and nondestructive estimation of anthocyanin content in plant leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXltVyks7c%3D&md5=23c4a25e3de9e702b8744b2b6f21d030CAS |

Gitelson AA, Zur Y, Chivkunova OB, Merzlyak MN (2002) Assessing carotenoid content in plant leaves with reflectance spectroscopy. Photochemistry and Photobiology 75, 272–281.
Assessing carotenoid content in plant leaves with reflectance spectroscopy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XivFGntLk%3D&md5=03a72025db36c5359a5369d702ea8cb7CAS |

Godfray HC, Beddington JR, Crute IR, Haddad L, Lawrence D, Muir JF, Pretty J, Robinson S, Thomas SM, Toulmin C (2010) Food security: the challenge of feeding 9 billion people. Science 327, 812–818.
Food security: the challenge of feeding 9 billion people.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhslWisLo%3D&md5=d9ff1a2cec0b1ee06fd564d71097dde5CAS |

Gómez S, Ferrieri RA, Schueller M, Orians CM (2010) Methyl jasmonate elicits rapid changes in carbon and nitrogen dynamics in tomato. New Phytologist 188, 835–844.
Methyl jasmonate elicits rapid changes in carbon and nitrogen dynamics in tomato.Crossref | GoogleScholarGoogle Scholar |

Good AG, Shrawat AK, Muench DG (2004) Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production? Trends in Plant Science 9, 597–605.
Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVaksLvM&md5=6011cfb7ae08b7ebb9b39f1cf245a5c6CAS |

Gowik U, Westhoff P (2011) The path from C3 to C4 photosynthesis. Plant Physiology 155, 56–63.
The path from C3 to C4 photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXksFagsL0%3D&md5=3543a8ad4e52a510777dcd50b4241b48CAS |

Gregory PJ (2006) ‘Plant roots.’ (Blackwell Publishing Ltd: Oxford)

Haacke EM, Brown RW, Thompson MR, Venkatesan R (1999) ‘Magnetic resonance imaging.’ (John Wiley & Sons: New York)

Haber A, Haber-Pohlmeier S, Casanova F, Blumich B (2010) Relaxation-Relaxation Experiments in Natural Porous Media with Portable Halbach Magnets. Vadose Zone Journal 9, 893–897.
Relaxation-Relaxation Experiments in Natural Porous Media with Portable Halbach Magnets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltVajtb0%3D&md5=b2e6c0e3ef07e775be4dc845baf4bf3bCAS |

Hammer GL, Dong Z, McLean G, Doherty A, Messina C, Schussler J, Zinselmeier C, Paszkiewicz S, Cooper M (2009) Can changes in canopy and/or root system architecture explain historical maize yield trends in the US corn belt? Crop Science 49, 299–312.
Can changes in canopy and/or root system architecture explain historical maize yield trends in the US corn belt?Crossref | GoogleScholarGoogle Scholar |

Hartley RI, Zisserman A (2004) ‘Multiple view geometry in computer vision.’ (Cambridge University Press: Cambridge, UK)

Hendricks JJ, Nadelhoffer KJ, Aber JD (1993) Assessing the role of fine roots in carbon and nutrient cycling. Trends in Ecology & Evolution 8, 174–178.
Assessing the role of fine roots in carbon and nutrient cycling.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itVylug%3D%3D&md5=e8d829fc6a4250fcf9839582bada4396CAS |

Herder GD, Isterdael GV, Beeckman T, De Smet I (2010) The roots of a new green revolution. Trends in Plant Science 15, 600–607.
The roots of a new green revolution.Crossref | GoogleScholarGoogle Scholar |

Hibberd JM, Sheehy JE, Langdale JA (2008) Using C4 photosynthesis to increase the yield of rice – rationale and feasibility. Current Opinion in Plant Biology 11, 228–231.
Using C4 photosynthesis to increase the yield of rice – rationale and feasibility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktFCmsLs%3D&md5=c63febccc6ae6adabd60552017733147CAS |

Hirel B, Le Gouis J, Ney B, Gallais A (2007) The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. Journal of Experimental Botany 58, 2369–2387.
The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXos1ykt74%3D&md5=060a0fbca0ad97e51e940521324f1e24CAS |

Hossain MM, Nonami H (2010) Effects of water flow from the xylem on the growth-induced water potential and the growth-effective turgor associated with enlarging tomato fruit. Environment Control in Biology 48, 101–116.
Effects of water flow from the xylem on the growth-induced water potential and the growth-effective turgor associated with enlarging tomato fruit.Crossref | GoogleScholarGoogle Scholar |

Houle D, Govindaraju DR, Omholt S (2010) Phenomics: the next challenge. Nature Reviews. Genetics 11, 855–866.
Phenomics: the next challenge.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVejs7jK&md5=08fb3c5b88385bf5df372ea31770143dCAS |

Hund A, Trachsel S, Stamp P (2009) Growth of axile and lateral roots of maize: I. Development of a phenotying platform. Plant and Soil 325, 335–349.
Growth of axile and lateral roots of maize: I. Development of a phenotying platform.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFSrt7vI&md5=09fa0807116a281710bd93a4cc731b5eCAS |

Jahnke S, Bier D, Estruch JJ, Beltran JP (1989) Distribution of photoassimilates in the pea plant: chronology of events in non-fertilized ovaries and effects of gibberellic acid. Planta 180, 53–60.
Distribution of photoassimilates in the pea plant: chronology of events in non-fertilized ovaries and effects of gibberellic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXlt1elsA%3D%3D&md5=a0995707d05df790e909c93704d72243CAS |

Jahnke S, Menzel MI, van Dusschoten D, Roeb GW, Bühler J, Minwuyelet S, Blümler P, Temperton VM, Hombach T, Streun M, Beer S, Khodaverdi M, Ziemons K, Coenen HH, Schurr U (2009) Combined MRI-PET dissects dynamic changes in plant structures and functions. The Plant Journal 59, 634–644.
Combined MRI-PET dissects dynamic changes in plant structures and functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFChtrrK&md5=10c7273c93e4a049e922b9f3131efbfdCAS |

Jansen M, Gilmer F, Biskup B, Nagel KA, Rascher U, Fischbach A, Briem S, Dreissen G, Tittmann S, Braun S, De Jaeger I, Metzlaff M, Schurr U, Scharr H, Walter A (2009) Simultaneous phenotyping of leaf growth and chlorophyll fluorescence via GROWSCREEN FLUORO allows detection of stress tolerance in Arabidopsis thaliana and other rosette plants. Functional Plant Biology 36, 902–914.
Simultaneous phenotyping of leaf growth and chlorophyll fluorescence via GROWSCREEN FLUORO allows detection of stress tolerance in Arabidopsis thaliana and other rosette plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlOgs7rF&md5=85fe567810d5e3477205ea5a4434545aCAS |

Kant S, Bi YM, Rothstein SJ (2011) Understanding plant response to nitrogen limitation for the improvement of crop nitrogen use efficiency. Journal of Experimental Botany 62, 1499–1509.
Understanding plant response to nitrogen limitation for the improvement of crop nitrogen use efficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1Gjsbs%3D&md5=5a372059222797783e680f13014958d2CAS |

Kao WY, Forseth IN (1991) The effect of nitrogen, light and water availability on tropic leaf movement in soybean (Glycine max). Plant, Cell & Environment 14, 287–293.
The effect of nitrogen, light and water availability on tropic leaf movement in soybean (Glycine max).Crossref | GoogleScholarGoogle Scholar |

Kao WY, Forseth IN (1992) Diurnal leaf movement, chlorophyll fluorescence and carbon assimilation in soybean grown under different nitrogen and water availabilities. Plant, Cell & Environment 15, 703–710.
Diurnal leaf movement, chlorophyll fluorescence and carbon assimilation in soybean grown under different nitrogen and water availabilities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xls1Oqtr4%3D&md5=0565731b8a928cf30e74f62b4cfa58e9CAS |

Kiyomiya S, Nakanishi H, Uchida H, Tsuji A, Nishiyama S, Futatsubashi M, Tsukada H, Ishioka NS, Watanabe S, Ito T, Mizuniwa C, Osa A, Matsuhashi S, Hashimoto S, Sekine T, Mori S (2001) Real time visualization of 13N-translocation in rice under different environmental conditions using positron emitting tracer imaging system. Plant Physiology 125, 1743–1753.
Real time visualization of 13N-translocation in rice under different environmental conditions using positron emitting tracer imaging system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtFKqtL8%3D&md5=c2897975c5d01aea23f6f8d0dbbd9885CAS |

Knoblauch M, Peters WS, Ehlers K, van Bel AJE (2001) Reversible calcium-regulated stopcocks in legume sieve tubes. The Plant Cell 13, 1221–1230.

Köckenberger W (2001) Functional imaging of plants by magnetic resonance experiments. Trends in Plant Science 6, 286–292.
Functional imaging of plants by magnetic resonance experiments.Crossref | GoogleScholarGoogle Scholar |

Kockenberger W, De Panfilis C, Santoro D, Dahiya P, Rawsthorne S (2004) High resolution NMR microscopy of plants and fungi. Journal of Microscopy 214, 182–189.
High resolution NMR microscopy of plants and fungi.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c3gsFajug%3D%3D&md5=85a783700ed11d7d51afc8b568634f4cCAS |

Kolber Z, Klimov D, Ananyev G, Rascher U, Berry JA, Osmond CB (2005) Measuring photosynthetic parameters at a distance: laser induced fluorescence transient (LIFT) method for remote measurements of PSII in terrestrial vegetation. Photosynthesis Research 84, 121–129.
Measuring photosynthetic parameters at a distance: laser induced fluorescence transient (LIFT) method for remote measurements of PSII in terrestrial vegetation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXms1yitrs%3D&md5=f5b54aca1d7ebe3462619c8addb397b4CAS |

Körner C (2011) The grand challenges in functional plant ecology. Frontiers in Plant Sciences 2, 1–3.
The grand challenges in functional plant ecology.Crossref | GoogleScholarGoogle Scholar |

Kuchenbrod E, Haase A, Benkert R, Schneider H, Zimmermann U (1995) Quantitative NMR microscopy on intact plants. Magnetic Resonance Imaging 13, 447–455.
Quantitative NMR microscopy on intact plants.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2MzhtFKktw%3D%3D&md5=0da89bbf69fad484ec489b4eb6abf0f7CAS |

Le Bot J, Serra V, Fabre J, Draye X, Adamowicz S, Pagès L (2010) DART: a software to analyse root system architecture and development from captured images. Plant and Soil 326, 261–273.
DART: a software to analyse root system architecture and development from captured images.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFGrt7jE&md5=55752bea5f6d84bf4178ad281780333fCAS |

Liu LY, Zhang YJ, Wang JH, Zhao CJ (2005) Detecting solar-induced chlorophyll fluorescence from field radiance spectra based on the Fraunhofer line principle. IEEE Transactions on Geoscience and Remote Sensing 43, 827–832.
Detecting solar-induced chlorophyll fluorescence from field radiance spectra based on the Fraunhofer line principle.Crossref | GoogleScholarGoogle Scholar |

Long SP, Ort DR (2010) More than taking the heat: crops and global change. Current Opinion in Plant Biology 13, 240–247.
More than taking the heat: crops and global change.Crossref | GoogleScholarGoogle Scholar |

Long SP, Zhu X-G, Naidu SL, Ort DR (2006) Can improvement in photosynthesis increase crop yields? Plant, Cell & Environment 29, 315–330.
Can improvement in photosynthesis increase crop yields?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xktlyltrw%3D&md5=9f5c649085a34b282eede80180c02b0cCAS |

Lynch JP, Jonathan P (2007) Roots of the second green revolution. Australian Journal of Botany 55, 493–512.
Roots of the second green revolution.Crossref | GoogleScholarGoogle Scholar |

Maier SW, Günther KP, Stellmes M (2003) Sun-induced fluorescence: a new tool for precision farming. In ‘Digital imaging and spectral techniques: applications to precision agriculture and crop physiology’. (Eds T van Toai, D Major, M McDonald, J Schepers, L Tarpley) pp. 209–222. (American Society of Agronomy: Madison, WI)

Malenovsky Z, Mishra KB, Zemek F, Rascher U, Nedbal L (2009) Scientific and technical challenges in remote sensing of plant canopy reflectance and fluorescence. Journal of Experimental Botany 60, 2987–3004.
Scientific and technical challenges in remote sensing of plant canopy reflectance and fluorescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpsValsbg%3D&md5=2cd4409b92442cfcc47a6916863efcb4CAS |

Masclaux-Daubresse C, Daniel-Vedele F, Dechorgnat J, Chardon F, Gaufichon L, Suzuki A (2010) Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Annals of Botany 105, 1141–1157.
Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture.Crossref | GoogleScholarGoogle Scholar |

Maxwell K, Johnson GN (2000) Chlorophyll fluorescence – a practical guide. Journal of Experimental Botany 51, 659–668.
Chlorophyll fluorescence – a practical guide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtF2js74%3D&md5=092bf5f89ae722b319a6295d4f24cbd4CAS |

Meroni M, Colombo R (2006) Leaf level detection of solar induced chlorophyll fluorescence by means of a subnanometer resolution spectroradiometer. Remote Sensing of Environment 103, 438–448.
Leaf level detection of solar induced chlorophyll fluorescence by means of a subnanometer resolution spectroradiometer.Crossref | GoogleScholarGoogle Scholar |

Meroni M, Rossini M, Guanter L, Alonso L, Rascher U, Colombo R, Moreno J (2009) Remote sensing of solar-induced chlorophyll fluorescence: review of methods and applications. Remote Sensing of Environment 113, 2037–2051.
Remote sensing of solar-induced chlorophyll fluorescence: review of methods and applications.Crossref | GoogleScholarGoogle Scholar |

Mittler R, Blumwald E (2010) Genetic engineering for modern agriculture: challenges and perspectives. Annual Review of Plant Biology 61, 443–462.
Genetic engineering for modern agriculture: challenges and perspectives.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnslSjsLc%3D&md5=834ce88b3b10f8445d8b288a4f51146fCAS |

Moll RH, Kamprath EJ, Jackson WA (1982) Analysis and interpretation of factors which contribute to efficiency of nitrogen utilization. Agronomy Journal 74, 562–564.
Analysis and interpretation of factors which contribute to efficiency of nitrogen utilization.Crossref | GoogleScholarGoogle Scholar |

Moya I, Camenen L, Evain S, Goulas Y, Cerovic ZG, Latouche G, Flexas J, Ounis A (2004) A new instrument for passive remote sensing 1. Measurements of sunlight-induced chlorophyll fluorescence. Remote Sensing of Environment 91, 186–197.
A new instrument for passive remote sensing 1. Measurements of sunlight-induced chlorophyll fluorescence.Crossref | GoogleScholarGoogle Scholar |

Mühlich M, Truhn D, Nagel KA, Walter A, Scharr H, Aach T (2008) Measuring plant root growth. In ‘Lecture notes in Computer Science 5096’. (Ed. G Rigoll) pp. 497–506. (Springer: Heidelberg, Germany)

Muller B, Stosser M, Tardieu F (1998) Spatial distributions of tissue expansion and cell division rates are related to irradiance and to sugar content in the growing zone of maize roots. Plant, Cell & Environment 21, 149–158.
Spatial distributions of tissue expansion and cell division rates are related to irradiance and to sugar content in the growing zone of maize roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjslGgtLc%3D&md5=d85de6f708962687a3cfdf0c4875aad2CAS |

Murchie EH, Pinto M, Horton P (2009) Agriculture and the new challenges for photosynthesis research. New Phytologist 181, 532–552.
Agriculture and the new challenges for photosynthesis research.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivFSls70%3D&md5=14d29d2e1a4f69f82e79fa3894a1824dCAS |

Nagel KA, Schurr U, Walter A (2006) Dynamics of root growth stimulation in Nicotiana tabacum in increasing light intensity. Plant, Cell & Environment 29, 1936–1945.
Dynamics of root growth stimulation in Nicotiana tabacum in increasing light intensity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1aktLjJ&md5=dcae25c8c7e05ac78bffe78e9f613ad5CAS |

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=4a68526c6c350fa9f16c551c5cbbbb3cCAS |

Nakanishi H, Kiyomiya S, Tsukamoto T, Tsukada H, Uchida H, Mori S (2002) Water (H215O) flow in rice is regulated by the concentration of nutrients as monitored by positron multi-probe system (PMPS). Soil Science and Plant Nutrition 48, 759–762.

Ohtake N, Sato T, Fujikake H, Sueyoshi K, Ohyama T, Ishioka NS, Watanabe S, Osa A, Sekine T, Matsuhashi S, Ito T, Mizuniwa C, Kume T, Hashimoto S, Uchida H, Tsuji A (2001) Rapid N transport to pods and seeds in N-deficient soybean plants. Journal of Experimental Botany 52, 277–283.
Rapid N transport to pods and seeds in N-deficient soybean plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtVajurg%3D&md5=9ac3d00b3053a931124b4d31f1f03ad1CAS |

Ohya T, Tanoi K, Hamada Y, Okabe H, Rai H, Hojo J, Suzuki K, Nakanishi TM (2008) An analysis of long-distance water transport in the soybean stem using H215O. Plant & Cell Physiology 49, 718–729.
An analysis of long-distance water transport in the soybean stem using H215O.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnvFWns70%3D&md5=dc21a18298518bc3fcf492f94fa0054dCAS |

Olson CF, Matthies LH, Wright JR, Li R, Di K (2007) Visual terrain mapping for mars exploration. Computer Vision and Image Understanding 105, 73–85.
Visual terrain mapping for mars exploration.Crossref | GoogleScholarGoogle Scholar |

Osmond CB, Björkman O, Anderson DJ (1980) ‘Physiological processes in plant ecology.’ (Springer: New York)

Parry MAJ, Andralojc PJ, Mitchell RAC, Madgwick PJ, Keys AJ (2003) Manupulation of Rubisco: the amount, activity, function and regulation. Journal of Experimental Botany 54, 1321–1333.
Manupulation of Rubisco: the amount, activity, function and regulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjt1Ogs7s%3D&md5=ddaf7758496fe6d20d68fb7de5327801CAS |

Pieruschka R, Klimov D, Kolber ZS, Berry JA (2010) Monitoring of cold and light stress impact on photosynthesis by using the laser induced fluorescence transient (LIFT) approach. Functional Plant Biology 37, 395–402.
Monitoring of cold and light stress impact on photosynthesis by using the laser induced fluorescence transient (LIFT) approach.Crossref | GoogleScholarGoogle Scholar |

Plascyk JA, Gabriel FC (1975) The Fraunhofer line discriminator MKII – an airborne instrument for precise and standardized ecological luminescence measurement. IEEE Transactions on Instrumentation and Measurement 24, 306–313.
The Fraunhofer line discriminator MKII – an airborne instrument for precise and standardized ecological luminescence measurement.Crossref | GoogleScholarGoogle Scholar |

Poorter H, Niinemets Ü, Walter A, Fiorani F, Schurr U (2010) A method to construct dose–response curves for a wide range of environmental factors and plant traits by means of a meta-analysis of phenotypic data. Journal of Experimental Botany 61, 2043–2055.
A method to construct dose–response curves for a wide range of environmental factors and plant traits by means of a meta-analysis of phenotypic data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmsVGgu7c%3D&md5=184d20864d5cb74cabca58d5d4d8887dCAS |

Rascher U, Nedbal L (2006) Dynamics of photosynthesis in fluctuating light – commentary. Current Opinion in Plant Biology 9, 671–678.
Dynamics of photosynthesis in fluctuating light – commentary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVygt7jF&md5=2f74693d8c6aa0a395430c1094b1c055CAS |

Rascher U, Pieruschka R (2008) Spatio-temporal variations of photosynthesis – the potential of optical remote sensing to better understand and scale light use efficiency and stresses of plant ecosystems. Precision Agriculture 9, 355–366.
Spatio-temporal variations of photosynthesis – the potential of optical remote sensing to better understand and scale light use efficiency and stresses of plant ecosystems.Crossref | GoogleScholarGoogle Scholar |

Rascher U, Nichol CJ, Small C, Hendricks L (2007) Monitoring spatio-temporal dynamics of photosynthesis with a portable hyperspectral imaging system. Photogrammetric Engineering and Remote Sensing 73, 45–56.

Rascher U, Agati G, Alonso L, Cecchi G, Champagne S, Colombo R, Damm A, Daumard F, de Miguel E, Fernandez G, Franch B, Franke J, Gerbig C, Gioli B, Gómez JA, Goulas Y, Guanter L, Gutiérrez-De-La-Cámara Ó, Hamdi K, Hostert P, Jiménez M, Kosvancova M, Lognoli D, Meroni M, Miglietta F, Moersch A, Moreno J, Moya I, Neininger B, Okujeni A, Ounis A, Palombi L, Raimondi V, Schickling A, Sobrino JA, Stellmes M, Toci G, Toscano P, Udelhoven T, van der Linden S, Zaldei A (2009) CEFLES2: the remote sensing component to quantify photosynthetic efficiency from the leaf to the region by measuring sun-induced fluorescence in the oxygen absorption bands. Biogeosciences 6, 1181–1198.
CEFLES2: the remote sensing component to quantify photosynthetic efficiency from the leaf to the region by measuring sun-induced fluorescence in the oxygen absorption bands.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1OhtLrL&md5=ce8488703056407719f2e38205c28e16CAS |

Rascher U, Biskup B, Leakey ADB, McGrath JM, Ainsworth EA (2010a) Altered physiological function, not structure, drives increased radiation-use efficiency of soybean grown at elevated CO2. Photosynthesis Research 105, 15–25.
Altered physiological function, not structure, drives increased radiation-use efficiency of soybean grown at elevated CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXntlGitLs%3D&md5=6e043e21e5c0de39086b80c8467ae618CAS |

Rascher U, Damm A, van der Linden S, Okujeni A, Pieruschka R, Schickling A, Hostert P (2010b) Sensing of photosynthetic activity of crops. In ‘Precision crop protection – the challenge and use of heterogeneity’. (Ed. EC Oerke) (Springer Science + Business Media BV: Dordrecht, The Netherlands)

Roeb G, Britz SJ (1991) Short-term fluctuations in the transport of assimilates to the ear of wheat measured with steady state 11C–CO2-labelling of the flag leaf. Journal of Experimental Botany 42, 469–475.
Short-term fluctuations in the transport of assimilates to the ear of wheat measured with steady state 11C–CO2-labelling of the flag leaf.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXisVCmsrc%3D&md5=d938ec1213aabbe258469a8374cc6420CAS |

Rogers A, Allen DJ, Davey PA, Morgan PB, Ainsworth EA, Bernacchi CJ, Cornic G, Dermody O, Dohleman FG, Heaton EA, Mahoney J, Zhu XG, Delucia EH, Ort DR, Long SP (2004) Leaf photosynthesis and carbohydrate dynamics of soybeans grown throughout their life-cycle under free-air carbon dioxide enrichment. Plant, Cell & Environment 27, 449–458.
Leaf photosynthesis and carbohydrate dynamics of soybeans grown throughout their life-cycle under free-air carbon dioxide enrichment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjs1ahtbs%3D&md5=37a7edb4f7c9514420bed616574e64f5CAS |

Roscher C, Thein S, Weigelt A, Temperton VM, Buchmann N, Schulze ED (2011) N2 fixation and performance of 12 legume species in a 6-year grassland biodiversity experiment. Plant and Soil 341, 333–348.
N2 fixation and performance of 12 legume species in a 6-year grassland biodiversity experiment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjt1Wjtro%3D&md5=f924b64515f810849b2044daae8dddc4CAS |

Rosema A, Snel JFH, Zahn H, Buurmeijer WF, van Hove LWA (1998) The relation between laser-induced chlorophyll fluorescence and photosynthesis. Remote Sensing of Environment 65, 143–154.
The relation between laser-induced chlorophyll fluorescence and photosynthesis.Crossref | GoogleScholarGoogle Scholar |

Scharr H (2007) Optimal filters for extended optical flow. In ‘LNCS 3417 International Workshop on Complex Motion’. pp. 14–29. (Springer: Heidelberg, Germany)

Schmundt D, Stitt M, Jähne B, Schurr U (1998) Quantitative analysis of the local rates of growth of dicot leaves at a high temporal and spatial resolution, using image sequence analysis. The Plant Journal 16, 505–514.
Quantitative analysis of the local rates of growth of dicot leaves at a high temporal and spatial resolution, using image sequence analysis.Crossref | GoogleScholarGoogle Scholar |

Schurr U, Walter A, Rascher U (2006) Functional dynamics of plant growth and photosynthesis - from steady-state to dynamics – from homogeneity to heterogeneity. Plant, Cell & Environment 29, 340–352.
Functional dynamics of plant growth and photosynthesis - from steady-state to dynamics – from homogeneity to heterogeneity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xktlyltro%3D&md5=a3892a1a27df8880ea332409acac740fCAS |

Sharp RE, Silk WK, Hsiao TC (1988) Growth of the maize primary root at low water potentials. 1. Spatial-distribution of expansive growth. Plant Physiology 87, 50–57.
Growth of the maize primary root at low water potentials. 1. Spatial-distribution of expansive growth.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnhvVartg%3D%3D&md5=18e8b7e8bf24f782e1c2312f10afeb71CAS |

Silk WK (1992) Steady form from changing cells. International Journal of Plant Sciences 153, S49–S58.
Steady form from changing cells.Crossref | GoogleScholarGoogle Scholar |

Sinclair TR, Muchow RC (1999) Radiation use efficiency. Advances in Agronomy 65, 215–265.
Radiation use efficiency.Crossref | GoogleScholarGoogle Scholar |

Sinclair TR, Muchow RC, Ludlow MM, Leach GJ, Lawn RJ, Foale MA (1987) Field and model analysis of the effect of water deficits on carbon and nitrogen accumulation by soybean, cowpea and black gram. Field Crops Research 17, 121–140.
Field and model analysis of the effect of water deficits on carbon and nitrogen accumulation by soybean, cowpea and black gram.Crossref | GoogleScholarGoogle Scholar |

Tambussi EA, Bort J, Araus JL (2007) Water use efficiency in C3 cereals under Mediterranean conditions: a review of physiological aspects. The Annals of Applied Biology 150, 307–321.
Water use efficiency in C3 cereals under Mediterranean conditions: a review of physiological aspects.Crossref | GoogleScholarGoogle Scholar |

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=38d8909b7db73079ae5c15775eb4a5e4CAS |

Tsukamoto T, Nakanishi H, Uchida H, Watanabe S, Matsuhashi S, Mori S, Nishizawa NK (2009) 52Fe translocation in barley as monitored by a positron-emitting tracer imaging system (PETIS): evidence for the direct translocation of Fe from roots to young leaves via phloem. Plant & Cell Physiology 50, 48–57.
52Fe translocation in barley as monitored by a positron-emitting tracer imaging system (PETIS): evidence for the direct translocation of Fe from roots to young leaves via phloem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVehurg%3D&md5=2d34cbf507be093c5ccc32e6a1d9066fCAS |

Tyree MT, Ewers FW (1991) The hydraulic architecture of trees and other woody-plants. New Phytologist 119, 345–360.
The hydraulic architecture of trees and other woody-plants.Crossref | GoogleScholarGoogle Scholar |

Ustin S, Gamon JA (2010) Remote sensing of plant functional types. New Phytologist 186, 795–816.
Remote sensing of plant functional types.Crossref | GoogleScholarGoogle Scholar |

Ustin SL, Roberts DA, Gamon JA, Asner GP, Green RO (2004) Using imaging spectroscopy to study ecosystem processes and properties. Bioscience 54, 523–534.
Using imaging spectroscopy to study ecosystem processes and properties.Crossref | GoogleScholarGoogle Scholar |

Van As H (2007) Intact plant MRI for the study of cell water relations, membrane permeability, cell-to-cell and long distance water transport. Journal of Experimental Botany 58, 743–756.
Intact plant MRI for the study of cell water relations, membrane permeability, cell-to-cell and long distance water transport.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXislCrt70%3D&md5=b0c17eb97c52072e0bd195d71a9e3ab0CAS |

Van As H, Scheenen T, Vergeldt FJ (2009) MRI of intact plants. Photosynthesis Research 102, 213–222.
MRI of intact plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVWhtrfM&md5=e5db09800781e336bc1a1cf30f3a9679CAS |

van Bel AJE (2003) Transport phloem: low profile, high impact. Plant Physiology 131, 1509–1510.

van der Mark W, Gavrila DM (2006) Real-time dense stereo for intelligent vehicles. IEEE Transactions on Intelligent Transportation Systems 7, 38–50.
Real-time dense stereo for intelligent vehicles.Crossref | GoogleScholarGoogle Scholar |

van der Tol C, Verhoef W, Rosema A (2009) A model for chlorophyll fluorescence and photosynthesis at leaf scale. Agricultural and Forest Meteorology 149, 96–105.
A model for chlorophyll fluorescence and photosynthesis at leaf scale.Crossref | GoogleScholarGoogle Scholar |

Walter A, Schurr U (2005) Dynamics of leaf and root growth: endogenous control versus environmental impact. Annals of Botany 95, 891–900.
Dynamics of leaf and root growth: endogenous control versus environmental impact.Crossref | GoogleScholarGoogle Scholar |

Walter A, Spies H, Terjung S, Küsters R, Kirchgeßner N, Schurr U (2002) Spatio-temporal dynamics of expansion growth in roots: automatic quantification of diurnal course and temperature response by digital image sequence processing. Journal of Experimental Botany 53, 689–698.
Spatio-temporal dynamics of expansion growth in roots: automatic quantification of diurnal course and temperature response by digital image sequence processing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitlCks7g%3D&md5=769fc2c47d14f0e8455facbbf69e73fcCAS |

Walter A, Silk WK, Schurr U (2009) Environmental effects on spatial and temporal patterns of leaf and root growth. Annual Review of Plant Biology 60, 279–304.
Environmental effects on spatial and temporal patterns of leaf and root growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntFGls7c%3D&md5=062f2149d103f94dbb9da98bb926f4e6CAS |

Watt M, Silk WK, Passioura JB (2006) Rates of root and organism growth, soil conditions, and temporal and spatial development of the rhizosphere. Annals of Botany 97, 839–855.
Rates of root and organism growth, soil conditions, and temporal and spatial development of the rhizosphere.Crossref | GoogleScholarGoogle Scholar |

Whitney SM, Houtz RL, Alonso H (2011) Advancing our understanding and capacity to engineer Nature’s CO2-sequestering enzyme, Rubisco. Plant Physiology 155, 27–35.
Advancing our understanding and capacity to engineer Nature’s CO2-sequestering enzyme, Rubisco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXksFags7c%3D&md5=7390d0e48339afd33350703cd16f0117CAS |

Windt CW, Vergeldt FJ, De Jager PA, Van As H (2006) MRI of long-distance water transport: a comparison of the phloem and xylem flow characteristics and dynamics in poplar, castor bean, tomato and tobacco. Plant, Cell and Environment 29, 1715–1729.
MRI of long-distance water transport: a comparison of the phloem and xylem flow characteristics and dynamics in poplar, castor bean, tomato and tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVWktLjO&md5=428adc24ff0c07a4e2bac27680144718CAS |

Windt CW, Gerkema E, Van As H (2009) Most water in the tomato truss is imported through the xylem, not the phloem: a nuclear magnetic resonance flow imaging study. Plant Physiology 151, 830–842.
Most water in the tomato truss is imported through the xylem, not the phloem: a nuclear magnetic resonance flow imaging study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlSjsr%2FP&md5=423c7e07409037c33108d9ad47d9c268CAS |

Windt CW, Soltner H, van Dusschoten D, Blümler P (2011) A portable Halbach magnet that can be opened and closed without force: the NMR-CUFF. Journal of Magnetic Resonance (San Diego, Calif.) 208, 27–33.
A portable Halbach magnet that can be opened and closed without force: the NMR-CUFF.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjvF2ktg%3D%3D&md5=23992830f43cf7e4f9f6cc14654b4020CAS |

Yamashita N, Koike N, Ishida A (2002) Leaf ontogenetic dependence of light acclimation in invasive and native subtropical trees of different successional status. Plant, Cell & Environment 25, 1341–1356.
Leaf ontogenetic dependence of light acclimation in invasive and native subtropical trees of different successional status.Crossref | GoogleScholarGoogle Scholar |

Zhu XG, Ort DR, Whitmarsh J, Long SP (2004) The slow reversibility of photosystem II thermal energy dissipation on transfer from high to low light may cause large losses in carbon gain by crop canopies: a theoretical analysis. Journal of Experimental Botany 55, 1167–1175.
The slow reversibility of photosystem II thermal energy dissipation on transfer from high to low light may cause large losses in carbon gain by crop canopies: a theoretical analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXksVagsrk%3D&md5=10cc508b4449bc7920283bb9f930e140CAS |

Zhu XG, Long SP, Ort DR (2010) Improving photosynthetic efficiency for greater yield. Annual Review of Plant Biology 61, 235–261.
Improving photosynthetic efficiency for greater yield.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnslSjsL8%3D&md5=07486c7da91af9cf1d6ece0377e33664CAS |