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Plant phenotyping: a perspective

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Abstract

Sustainable agriculture for feeding increasing population is a foremost global challenge. The “green revolution” based crop productivity has done wonders in the past, but it has limits, and, thus, we are compelled to look for new avenues to increase productivity of important crops. Plant phenomics is emerging as a promising area in which many imaging sensors developed in the past are being tested for mapping of genetic information expressed within plant phenotypes, and the integrated use of these sensors may help speed-up unraveling of underlying molecular, biochemical and physiological mechanisms. We provide here a review of methods used for phenotyping and understanding of abiotic stress (drought/cold) tolerance mechanisms in the context of dynamic challenges faced by plants during their life.

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References

  • Amato, M., Bitella, G., Rossi, R., Gomez, J. A., Lovelli, S., & Gomes, J. J. F. (2009). Multi-electrode 3D resistivity imaging of alfalfa root zone. European Journal of Agronomy, 31, 213–222.

    Article  Google Scholar 

  • Athanasiou, K., Dyson, B. C., Webster, R. E., & Johnson, G. N. (2010). Dynamic acclimation of photosynthesis increases plant fitness in changing environments. Plant Physiology, 152, 366–373.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baker, N. R. (2008). Chlorophyll fluorescence: A probe of photosynthesis in vivo. Annual Review of Plant Biology, 59, 89–113.

    Article  CAS  PubMed  Google Scholar 

  • Banik, P., Zeng, W., Bizimungu, B., & Tanino, K. (2016). Effects of drought acclimation on drought stress resistance in potato (Solanum tuberosum L.) genotypes. Environmental and Experimental Botany, 126, 76–89.

    Article  Google Scholar 

  • Bates, G. H. (1937). A device for the observation of root growth in the soil. Nature, 139, 966–967.

    Article  Google Scholar 

  • Bauriegel, E., & Herppich, W. (2014). Hyperspectral and chlorophyll fluorescence imaging for early detection of plant diseases, with special reference to Fusarium spec. infections on wheat. Agriculture, 4, 32–57.

    Article  CAS  Google Scholar 

  • Bellasio, C., Olenickova, J., Tesar, R., Sebela, D., & Nedbal, L. (2012). Computer reconstruction of plant growth and chlorophyll fluorescence emission in three spatial dimensions. Sensors, 12(1), 1052–1071.

    Article  PubMed  PubMed Central  Google Scholar 

  • Berger, B., Parent, B., & Tester, M. (2010). High-throughput shoot imaging to study drought responses. Journal of Experimental Botany, 61, 3519–3528.

    Article  CAS  PubMed  Google Scholar 

  • Bilger, W., & Bjorkman, O. (1990). Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbency changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynthesis Research, 25, 173–185.

    Article  CAS  PubMed  Google Scholar 

  • Blum, A., Mayer, J., & Gozlan, G. (1982). Infrared thermal sensing of plant canopies as a screening technique for dehydration avoidance in wheat. Field Crops Research, 5, 137–146.

    Article  Google Scholar 

  • Bohm, W. (1979). Methods of studying root systems. Berlin: Springer.

    Book  Google Scholar 

  • Borhan, M. H., Holub, E. B., Beynon, J. L., Rozwadowski, K., & Rimmer, S. R. (2004). The Arabidopsis TIR-NB-LRR gene RAC1 confers resistance to Albugo candida (white rust) and is dependant on EDS1 but not PAD4. Molecular Plant-Microbe Interactions, 17, 711–719.

    Article  CAS  PubMed  Google Scholar 

  • Boyer, J. S. (2010). Drought decision-making. Journal of Experimental Botany, 61, 3493–3497.

    Article  CAS  PubMed  Google Scholar 

  • Buschmann, C. (2007). Variability and application of chlorophyll fluorescence emission ratio red/far-red of leaves. Photosynthesis Research, 92, 261–271.

    Article  CAS  PubMed  Google Scholar 

  • Buschmann, C., Langsdorf, G., & Lichtenthaler, H. K. (2000). Imaging of the blue, green, and red fluorescence emission of plants: An overview. Photosynthetica, 38, 483–491.

    Article  CAS  Google Scholar 

  • Caldana, C., Degenkolbe, T., Cuadros-Inostroza, A., Klie, S., Sulpice, R., Leisse, A., et al. (2011). High-density kinetic analysis of the metabolomic and transcriptomic response of Arabidopsis to eight environmental conditions. The Plant Journal, 67, 869–884.

    Article  CAS  PubMed  Google Scholar 

  • Campbell, B. (2013). The global imperative: Drought affects us all. Nature, 501, S12–S14.

    Article  CAS  Google Scholar 

  • Care, A. F., Nefedév, L., Bonnet, B., Millet, B., & Badot, P. M. (1998). Cell elongation and revolving movement in Phaseolus vulgaris L. twining shoots. Plant Cell Physiology, 39, 914–921.

    Article  CAS  Google Scholar 

  • Catalá, R., Medina, J., & Salinas, J. (2011). Integration of low temperature and light signaling during cold acclimation response in Arabidopsis. Proceedings of National Academy of Sciences USA, 108(39), 16475–16480.

    Article  Google Scholar 

  • Cerovic, Z. G., Samson, G., Morales, F., Tremblay, N., & Moya, I. (1999). Ultraviolet-induced fluorescence for plant monitoring: Present state and prospects. Agronomie, 19, 543–578.

    Article  Google Scholar 

  • Chaerle, L., Hagenbeek, D., De Bruyne, E., Valcke, R., & Van Der Straeten, D. (2004). Thermal and chlorophyll-fluorescence imaging distinguish plant–pathogen interactions at an early stage. Plant and Cell Physiology, 45, 887–896.

    Article  CAS  PubMed  Google Scholar 

  • Chappelle, E. W., McMurtrey, J. E., Wood, F. M., & Newcomb, W. W. (1984). Laser-induced fluorescence of green plants. 2. LIF caused by nutrient deficiencies in corn. Applied Optics, 23, 139–142.

    Article  CAS  PubMed  Google Scholar 

  • Chen, D., Wang, S., Xiong, B., Cao, B., & Deng, X. (2015). Carbon/Nitrogen imbalance associated with drought-induced leaf senescence in drought-induced leaf senescence in Sorghum bicolor. PLoS ONE, 10(8), e0137026.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Costa, J. M., Grant, O. M., & Chaves, M. M. (2013). Thermography to explore plant–environment interactions. Journal of Experimental Botany, 64, 3937–3949.

    Article  CAS  PubMed  Google Scholar 

  • Cruz, J. A., Savage, L. J., Zegarac, R., Kovac, W. K., Chen, J., & Kramer, D. M. (2016). Dynamic environmental photosynthetic imaging reveals emergent phenotypes. Cell Systems, 2, 365–377.

    Article  PubMed  Google Scholar 

  • Curran, P. J., Dungan, J. L., Macler, B. A., Plummer, S. E., & Peterson, D. L. (1992). Reflectance spectroscopy of fresh whole leaves for the estimation of chemical concentration. Remote Sensing of Environment, 39, 153–166.

    Article  Google Scholar 

  • Dau, H. (1994). Molecular mechanisms and quantitative models of variable photosystem II fluorescence. Photochemical and Photobiology, 60, 1–23.

    Article  CAS  Google Scholar 

  • Degenkolbe, T., Giavalisco, P., Zuther, E., Seiwert, B., Hincha, D. K., & Willmitzer, L. (2012). Differential remodeling of the lipidome during cold acclimation in natural accessions of Arabidopsis thaliana. The Plant Journal, 72, 972–982.

    Article  CAS  PubMed  Google Scholar 

  • Dhondt, S., Wuyts, N., & Inze, D. (2013). Cell to whole-plant phenotyping: the best is yet to come. Trends in Plant Science, 18, 428–439.

    Article  CAS  PubMed  Google Scholar 

  • Fahlgren, N., Gehan, M. A., & Baxter, I. (2015). Lights, camera, action: High-throughput plant phenotyping is ready for a close-up. Current Opinion in Plant Biology, 24, 93–99.

    Article  PubMed  Google Scholar 

  • Fiorani, F., & Schurr, U. (2013). Future scenarios for plant phenotyping. Annual Review of Plant Biology, 64, 267–291.

    Article  CAS  PubMed  Google Scholar 

  • Flood, P. J., Kruijer, W., Schnabel, S. K., van der Schoor, R., Jalink, H., Snel, J. F. H., Harbinson, J. & Arts, M.G.M. (2016). Phenomics for photosynthesis, growth and reflectance in Arabidopsis thaliana reveals circadian and long-term fluctuations in heritability. Plant Methods, 12, 14.

    Article  PubMed  PubMed Central  Google Scholar 

  • Fresco, L. O. (2015). The new green revolution: Bridging the gap between science and society. Current Science, 109(3), 430–438.

    Google Scholar 

  • Furbank, R. T., & Tester, M. (2011). Phenomics—technologies to relieve the phenotyping bottleneck. Trends Plant Science, 16, 635–644.

    Article  CAS  Google Scholar 

  • Gamon, J. A., Field, C. B., Bilger, W., Bjorkman, O., Fredeen, A. L., & Penuelas, J. (1990). Remote-sensing of the xanthophyll cycle and chlorophyll fluorescence in sunflower leaves and canopies. Oecologia, 85, 1–7.

    Article  Google Scholar 

  • Gamon, J. A., Penuelas, J., & Field, C. B. (1992). A narrow-waveband spectral index that tracks diurnal changes in photosynthetic efficiency. Remote Sensing of Environment, 41, 35–44.

    Article  Google Scholar 

  • Gates, D. M., Keegan, H. J., Schleter, J. C., & Weidner, V. R. (1965). Spectral properties of plants. Applied Optics, 4, 11–20.

    Article  Google Scholar 

  • Gitelson, A. A., Gritz, Y., & Merzlyak, M. N. (2003). Relationships between leaf chlorophyll content and spectral reflectance and algorithms for nondestructive chlorophyll assessment in higher plant leaves. Journal of Plant Physiology, 160, 271–282.

    Article  CAS  PubMed  Google Scholar 

  • Gitelson, A. A., Keydan, G. P., & Merzlyak, M. N. (2006). Three-band model for noninvasive estimation of chlorophyll, carotenoids, and anthocyanin contents in higher plant leaves. Geophysical Research Letters, 33, L11402. doi:10.1029/2006GL026457

    Article  CAS  Google Scholar 

  • Govindjee, (1995). Sixty-three years since Kautsky: Chlorophyll a fluorescence. Australian Journal of Plant Physiology, 22, 131–160.

    Article  CAS  Google Scholar 

  • Govindjee, (2004). Chlorophyll a fluorescence: A bit of basics and history. In G. C. Papageorgiou & Govindjee (Eds.), Chlorophyll a fluorescence: A signature of photosynthesis (pp. 2–42). Dordrecht, The Netherlands: Kluwer Academic.

    Google Scholar 

  • Govindjee, Amesz, J., & Fork, D. C. (Eds.). (1986). Light emission by plants and bacteria. New York (now Elsevier, Inc): Academic Press.

    Google Scholar 

  • Govindjee, Wong, D., Prezelin, B. B., & Sweeney, B. M. (1979). Chlorophyll a fluorescence of Gonyaulax polydera grown on a light-dark cycle and after transfer to constant light. Photochemical and Photobiology, 30, 405–411.

    Article  CAS  Google Scholar 

  • Granier, C., Aguirrezabal, L., Chenu, K., Cookson, S. J., Dauzat, M., Hamard, P., et al. (2006). PHENOPSIS, an automated platform for reproducible phenotyping of plant responses to soil water deficit in Arabidopsis thaliana permitted the identification of an accession with low sensitivity to soil water deficit. New Phytologist, 169, 623–635.

    Article  PubMed  Google Scholar 

  • Granier, C., & Vile, D. (2014). Phenotyping and beyond: Modelling the relationships between traits. Current Opinion in Plant Biology, 18, 96–102.

    Article  PubMed  Google Scholar 

  • Groom, Q. J., Kramer, D. M., Crofts, A. R., & Ort, D. R. (1993). The non-photochemical reduction of plastoquinone in leaves. Photosynthesis Research, 36, 205–215.

    Article  CAS  PubMed  Google Scholar 

  • Großkinsky, D. K., Pieruschka, R., Svensgaard, J., Rascher, U., Christensen, S., Schurr, U., et al. (2015). Phenotyping in the fields: Dissecting the genetics of quantitative traits and digital farming. New Phytologist, 207, 950–952.

    Article  PubMed  Google Scholar 

  • Haghighattalab, A., Pérez, L. G., Mondal, S., Singh, D., Schinstock, D., Rutkoski, J., et al. (2016). Application of unmanned aerial systems for high throughput phenotyping of large wheat breeding nurseries. Plant Methods, 12, 35.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hannah, M. A., Wiese, D., Freund, S., Fiehn, O., Heyer, A. G., et al. (2006). Natural genetic variation of freezing tolerance in Arabidopsis. Plant Physiology, 142, 98–112.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hargreaves, C., Gregory, P., & Bengough, A. (2009). Measuring root traits in barley (Hordeum vulgare ssp. vulgare and ssp. spontaneum) seedlings using gel chambers, soil sacs and X-ray microtomography. Plant and Soil, 316, 285–297.

    Article  CAS  Google Scholar 

  • Hartmann, A., Czauderna, T., Hoffmann, R., Stein, N., & Schreiber, F. (2011). HTPheno: An image analysis pipeline for high-throughput plant phenotyping. BMC Bioinformatics, 12, 148.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hashimoto, Y., Ino, T., Kamer, P. J., Naylor, A. W., & Strain, B. R. (1984). Dynamic analysis of water stress of sunflower leaves by means of a thermal image processing system. Plant Physiology, 76, 266–269.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoffmann, M. H. (2005). Evolution of the realized climatic niche in the genus Arabidopsis (Brassicaceae). Evolution, 59, 1425–1436.

    PubMed  Google Scholar 

  • Holub, O., Seufferheld, M. J., Gohlke, C., Govindjee, Heiss, & G.J. & Clegg, R.M., (2007). Flourescence lifetime imaging microscopy of Chlamydomonas reinhardtii: non-photochemical quenching mutants and the effect of photosynthetic inhibitors on the slow chlorophyll fluorescence transient. Journal of Microscopy, 226, 90–120.

    Article  CAS  PubMed  Google Scholar 

  • Houle, D. (2010). Numbering the hairs on our heads: The shared challenge and promise of phenomics. Proceedings of National Academy Sciences USA, 107, 1793–1799.

    Article  CAS  Google Scholar 

  • Houle, D., Govindaraju, D. R., & Omholt, S. (2010). Phenomics: The next challenge. Nature Reviews Genetics, 11, 855–866.

    Article  CAS  PubMed  Google Scholar 

  • Humplík, J. F., Lazár, D., Husičková, A., & Spíchal, L. (2015). Automated phenotyping of plant shoots using imaging methods for analysis of plant stress responses—a review. Plant Methods, 11, 29.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hund, A., Trachsel, S., & Stamp, P. (2009). Growth of axile and lateral roots of maize: I. Development of a phenotyping platform. Plant and Soil, 325, 335–349.

    Article  CAS  Google Scholar 

  • Jahnke, S., Menzel, M. I., Van Dusschoten, D., Roeb, G. W., Bühler, J., Minwuyelet, S., et al. (2009). Combined MRI–PET dissects dynamic changes in plant structures and functions. The Plant Journal, 59, 634–644.

    Article  CAS  PubMed  Google Scholar 

  • Jansen, M., Gilmer, F., Biskup, B., Nagel, K. A., Rascher, U., Fischbach, A., et al. (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.

    Article  CAS  Google Scholar 

  • Johannsen, W. (1911). The genotype conception of heredity. The American Naturalist, 45, 129–159.

    Article  Google Scholar 

  • Jones, H. G., Serraj, R., Loveys, B. R., Xiong, L., Wheaton, A., & Price, A. H. (2009). Thermal infrared imaging of crop canopies for the remote diagnosis and quantification of plant responses to water stress in the field. Functional Plant Biology, 36, 978–989.

    Article  Google Scholar 

  • Juszczak, I., Cvetkovic, J., Zuther, E., Hincha, D. K., & Baier, M. (2016). Natural variation of cold deacclimation correlates with variation of cold-acclimation of the plastid antioxidant system in Arabidopsis thaliana accessions. Frontiers in Plant Science, 7, 305.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kalaji, H. M., Schansker, G., Ladle, R. J., Goltsev, V., Bosa, K., Allakhverdiev, S. I., Bresric, M., et al. (2014). Frequently asked questions about chlorophyll fluorescence: Practical issues. Photosynthesis Research, 122(2), 121–158.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalaji, H. M., Schansker, G., Brestic, M., Bussoti, F., Calatayud, A., Ferroni, L., Goltsev, V., Guidi, L., Jajoo, A., Li, P., Losciale, P., Mishra, V. K., Misra, A. N., Nebauer, S. G., Pancaldi, S., Penella, C., Pollastrini, M., Suresh, K., Tambussi, E., Yanniccari, M., Zivcak, M., Cetner, M. D., Samborska, I. A., Stirbet, A., Olsovska, K., Kunderlikova, K., Shelonzek, H., Rusinowski, S., Bąba, W. (2016). Frequently asked questions about chlorophyll fluorescence, the sequel. Photosynthesis Research. doi:10.1007/s11120-016-0318-y.

    PubMed  Google Scholar 

  • Kandoi, D., Mohanty, S., Govindjee & Tripathy, B.C. (2016). Towards efficient photosynthesis: overexpression of Zea mays phosphoenolpyruvate carboxylase in Arabidopsis thaliana. Photosynthesis Research. doi:10.1007/s11120-016-0207-9.

    PubMed  Google Scholar 

  • Kesavan, P. C., & Malarvannan, S. (2014). Green to evergreen revolution: Ecological and evolutionary perspectives in pest management. Current Science, 99(7), 908–914.

    Google Scholar 

  • Kim, S. J., Deng, F., & Brown, M. S. (2011). Visual enhancement of old documents with hyperspectral imaging. Pattern Recognition, 44(7), 1461–1469.

    Article  Google Scholar 

  • Klem, K., Mishra, K. B., Novotná, K., Rapantová, B., Hodaňová, P., Mishra, A., Kovac, D., & Urban, O. (2016). Distinct growth and physiological responses of Arabidopsis thaliana accessions to drought stress and their detection using spectral reflectance and thermal imaging. Functional Plant Biology. doi:10.1071/FP16194.

    Google Scholar 

  • Koornneef, M., & Meinke, D. (2010). The development of Arabidopsis as a model plant. The Plant Journal, 61, 909–921.

    Article  CAS  PubMed  Google Scholar 

  • Kromdijk, J., Głowacka, K., Leonelli, L., Gabilly, S. T., Iwai, M., Niyogi, K. K., & Long, S.P. (2016). Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science, 354(6314), 857–860.

    Article  CAS  PubMed  Google Scholar 

  • Kuhlgert, S., Austic, G., Zegarac, R., Osei-Bonsu, I., Hoh, D., Chilvers, M. I., et al. (2016). MultispeQ Beta: A tool for large-scale plant phenotyping connected to the open PhotosynQ network. doi:10.1098/rsos.160592.

    Google Scholar 

  • Kulheim, C., Agren, J., & Jansson, S. (2002). Rapid regulation of light harvesting and plant fitness in the field. Science, 297, 91–93.

    Article  PubMed  Google Scholar 

  • Kulheim, C., & Jansson, S. (2005). What leads to reduced fitness in non-photochemical quenching mutants? Physiologia Plantarum, 125, 202–211.

    Article  CAS  Google Scholar 

  • Leister, D., Varotto, C., Pesaresi, P., et al. (1999). Large-scale evaluation of plant growth in Arabidopsis thaliana by non-invasive image analysis. Plant Physiology and Biochemistry., 37, 671–678.

    Article  CAS  Google Scholar 

  • Liebisch, F., Kirchgessner, N., Schneider, D., Walter, A., & Hund, A. (2015). Remote, aerial phenotyping of maize traits with a mobile multi-sensor approach. Plant Methods, 11, 9.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lobell, D. B., Schlenker, W., & Costa-Roberts, J. (2011). Climate trends and global crop production since 1980. Science, 333, 616–620.

    Article  CAS  PubMed  Google Scholar 

  • Lobet, G., Pagés, L., & Draye, X. (2011). A novel image-analysis toolbox enabling quantitative analysis of root system architecture. Plant Physiology, 157, 29–39.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lukas, V., Mishra, A., Mishra, K. B., & Hajslova, J. (2013). Mass spectrometry-based metabolomic fingerprinting for screening cold tolerance in Arabidopsis thaliana accessions. Analytical and Bioanalytical Chemistry, 405(8), 2671–2683.

    Article  CAS  Google Scholar 

  • Lynch, M., & Walsh, B. (1998). Genetics and analysis of quantitative traits. Sunderland, MA: Sinauer Associates.

    Google Scholar 

  • Mahlein, A. K., Oerke, E. C., Steiner, U., & Dehne, H. W. (2012). Recent advances in sensing plant diseases for precision crop protection. European Journal of Plant Pathology, 133, 197–209.

    Article  CAS  Google Scholar 

  • Malenovský, Z., Mishra, K. B., 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.

    Article  PubMed  CAS  Google Scholar 

  • Matouš, K., Benediktyova, Z., Berger, S., Roitsch, T., & Nedbal, L. (2006). Case study of combinatorial imaging: What protocol and what chlorophyll fluorescence image to use when visualizing infection of Arabidopsis thaliana by Pseudomonas syringae? Photosynthesis Research, 90, 243–253.

    Article  PubMed  CAS  Google Scholar 

  • Mishra, K. B., & Gopal, R. (2008). Detection of nickel-induced stress using laser-induced fluorescence signatures from leaves of wheat seedlings. International Journal of Remote Sensing, 29, 157–183.

    Article  Google Scholar 

  • Mishra, A., Heyer, A. G., & Mishra, K. B. (2014). Chlorophyll fluorescence emission can screen cold tolerance of cold acclimated Arabidopsis thaliana accessions. Plant Methods, 10, 38.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mishra, K. B., Iannacone, R., Petrozza, A., Mishra, A., Armentano, N., Vecchia, G. L., et al. (2012). Engineered drought tolerance in tomato plants is reflected in chlorophyll fluorescence emission. Plant Science, 182, 79–86.

    Article  CAS  PubMed  Google Scholar 

  • Mishra, A., Matouš, K., Mishra, K. B., & Nedbal, L. (2009). Towards discrimination of plant species by machine vision: Advanced statistical analysis of chlorophyll fluorescence transients. Journal of Fluorescence, 19, 905–913.

    Article  CAS  PubMed  Google Scholar 

  • Mishra, A., Mishra, K. B., Höermiller, I. I., Heyer, A. G., & Nedbal, L. (2011). Chlorophyll fluorescence emission as a reporter on cold tolerance in Arabidopsis thaliana accessions. Plant Signaling and Behaviour, 6(2), 301–310.

    Article  CAS  Google Scholar 

  • Mishra, K. B., Mishra, A., Novotná, K., Rapantová, B., Hodaňová, P., Urban, O., et al. (2016). Chlorophyll a fluorescence, under half of the adaptive growth-irradiance, for high-throughput sensing of leaf-water deficit in Arabidopsis thaliana accessions. Plant Methods, 12, 46. doi:10.1186/s13007-016-0145-3.

    Article  PubMed  PubMed Central  Google Scholar 

  • Moellering, E. R., Muthan, B., & Benning, C. (2010). Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science, 330(6001), 226–228.

    Article  CAS  PubMed  Google Scholar 

  • Morales, F., Cerovic, Z. G., & Moya, I. (1996). Time-resolved blue–green fluorescence of sugar beet (Beta vulgaris L.) leaves. Spectroscopic evidence for the presence of ferulic acid as the main fluorophore of the epidermis. Biochimica et Biophysica Acta, 1273, 251–262.

    Article  Google Scholar 

  • Munns, R., James, R., Sirault, X. R. R., Furbank, R. T., & Jones, H. G. (2010). New phenotyping methods for screening wheat and barley for beneficial responses to water deficit. Journal of Experimental Botany, 61, 3499–3507.

    Article  CAS  PubMed  Google Scholar 

  • Murchie, E. H., & Niyogi, K. K. (2011). Manipulation of photoprotection to improve plant photosynthesis. Plant Physiology, 155, 86–92.

    Article  CAS  PubMed  Google Scholar 

  • Nägel, K. A., Kastenholz, B., Jahnke, S., van-Dusschoten, D., Aach, T., Mühlich, M., et al. (2009). Temperature responses of roots: Impact on growth, root system architecture and implications for phenotyping. Functional Plant Biology, 36, 947–959.

    Article  CAS  Google Scholar 

  • Nedbal, L., & Whitmarsh, J. (2004). Chlorophyll fluorescence imaging of leaves and fruits. In G. C. Papageorgiou & Govindjee (Eds.), Chlorophyll a fluorescence: a signature of photosynthesis (pp. 389–407). Dordrecht, The Netherlands: Kluwer Academic.

    Chapter  Google Scholar 

  • Nelson, A. J., & Evans, M. L. (1986). Analysis of growth patterns during gravitropic curvature in roots of Zea mays by use of a computer based video digitizer. Journal of Plant Growth Regulator, 5, 73–84.

    Article  CAS  Google Scholar 

  • Omasa, K., Hosoi, F., & Konishi, A. (2007). 3D lidar imaging for detecting and understanding plant responses and canopy structure. Journal of Experimental Botany, 58, 881–898.

    Article  CAS  PubMed  Google Scholar 

  • Ort, D. R., Merchant, S. S., Alric, J., Barkan, A., Blankenship, R. E., Bock, R., et al. (2015). Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proceedings of National Academy of Sciences USA, 112, 8529–8536.

    Article  CAS  Google Scholar 

  • Oukarroum, A., & Strasser, R. J. (2004). Phenotyping of dark and light adapted barley plants by the fast chlorophyll a fluorescence rise OJIP. South African Journal of Botany, 70(2), 277–283.

    Article  CAS  Google Scholar 

  • Papageorgiou, G. C., & Govindjee, (Eds.). (2004). Chlorophyll a fluorescence: A signature of photosynthesis. Advances in photosynthesis and respiration (Vol. 19). Dordrecht: Springer.

    Google Scholar 

  • Paulus, S., Behmann, J., Mahlein, A. K., Plümer, L., & Kuhlmann, H. (2014). Low-cost 3D systems: Suitable tools for plant phenotyping. Sensors (Basel), 14, 3001–3018.

    Article  Google Scholar 

  • Perlikowski, D., Czyzniejewski, M., Marczak, Ł., Augustyniak, A., & Kosmala, A. (2016). Water deficit affects primary metabolism differently in two Lolium multiflorum/Festuca arundinacea introgression forms with a distinct capacity for photosynthesis and membrane regeneration. Frontiers in Plant Science. doi:10.3389/fpls.2016.01063.

    Google Scholar 

  • Pingali, P. L. (2012). Green revolution: Impacts, limits, and the path ahead. Proceedings of National Academy of Sciences USA, 109(31), 12302–12308.

    Article  CAS  Google Scholar 

  • Poorter, H., Fiorani, F., Pieruschka, R., Wojciechowski, T., Putten, W.H.V., et al. (2016). Pampered inside, pesteredoutside? Differences and similarities between plants growing in controlled conditions and in the field. New Phytologist. doi:10.1111/nph.1424.

  • Provart, N. J., Alonso, J., Assmann, S. M., Bergmann, D., Brady, S. M., Brkljacic, J., et al. (2016). 50 years of Arabidopsis research: highlights and future directions. New Phytologist, 209(3), 921–944.

    Article  CAS  PubMed  Google Scholar 

  • Pudil, P., Novovicova, J., & Kittler, J. (1994). Floating search methods in feature selection. Pattern Recognition Letters, 15, 1119–1125.

    Article  Google Scholar 

  • Rajendran, K., Tester, M., & Roy, S. J. (2009). Quantifying the three main components of salinity tolerance in cereals. Plant, Cell and Environment, 32, 237–249.

    Article  CAS  PubMed  Google Scholar 

  • Rascher, U., & Nedbal, L. (2006). Dynamics of photosynthesis in fluctuating light. Current Opinion in Plant Biology, 9, 671–678.

    Article  CAS  PubMed  Google Scholar 

  • Rattanapichai, W., & Klem, K. (2016). Two-dimensional root phenotyping system based on root growth on black filter paper and recirculation micro-irrigation. Czech Journal of Genetics and plant Breeding, 52, 64–70.

    Article  Google Scholar 

  • Ray, D. K., Mueller, N. D., West, P. C., & Foley, J. A. (2013). Yield trends are insufficient to double global crop production by 2050. PloS ONE, 8(6), e66428.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reuzeau, C., Pen, J., Frankard, V., de Wolf, J., Peerbolte, R., Broekaert, W., et al. (2005). TraitMill™: A discovery engine for identifying yield enhancement genes in cereals. Molecular Plant Breeding, 5, 753–759.

    Google Scholar 

  • Rhew, I. C., Stoep, A. V., Kearney, A., Smith, N. L., & Dunbar, M. D. (2011). Validation of the Normalized Difference Vegetation Index as a measure of neighborhood greenness. Annals of Epidemiology, 21(12), 946–952.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rouse, J. W. J., Haas, R. H., Schell, J. A., & Deering, D. W. (1974). Monitoring vegetation systems in the Great Plains with ERTS. In Freden, S. C., Marcanti, E. P., Becker, M. A. (Eds.), NASA SP-351. Proceedings of the 3rd Earth resources technology satellite-1 symposium, 1973 (pp. 309–317). Washington, DC: NASA Scientific and Technical Information Office.

  • Rousseau, D., Chéné, Y., Belin, E., Semaan, G., Trigui, G., Boudehri, K., et al. (2015). Multiscale imaging of plants: Current approaches and challenges. Plant Methods, 11, 6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruban, A. V. (2016). Nonphotochemical chlorophyll fluorescence quenching: Mechanism and effectiveness in protecting plants from photodamage. Plant Physiology, 170(4), 1903–1916.

    Article  CAS  PubMed  Google Scholar 

  • Rutherford, A. W., Govindjee, & Inoue, Y. (1984). Charge accumulation and photochemistry in leaves studied by thermoluminescence and delayed light emission. Proceedings of National Academy of Sciences USA, 81, 1107–1111.

    Article  CAS  Google Scholar 

  • Salvatori, E., Fu, S., & Man, F. (2016). Chlorophyll fluorescence for phenotyping drought-stressed trees in a mixed deciduous forest. Ann Bot (Roma), 6, 39–49.

    Google Scholar 

  • Seeing, H. D., Hoehn, A., Stodieck, L. S., Klaus, D. M., Adams, W. W., III, & Emery, W. J. (2009). Plant water parameters and the remote sensing R (1300)/R (1450) leaf water index: Controlled condition dynamics during the development of water deficit stress. Irrigation Science, 27(5), 357–365.

    Article  Google Scholar 

  • Skirycz, A., Vandenbroucke, K., Clauw, P., Maleux, K., Meyer, B. D., Dhondt, S., et al. (2011). Survival and growth of Arabidopsis plants given limited water are not equal. Nature Biotechnology, 29(3), 212–214.

    Article  CAS  PubMed  Google Scholar 

  • Smith, M. A. L., & Spomer, L. A. (1987). Direct quantification of in vitro cell growth through image analysis. In Vitro Cellular and Developmental Biology, 23, 67–74.

    Article  CAS  PubMed  Google Scholar 

  • Smith, M. A. L., Spomer, L. A., Meyer, M. J., & McClelland, M. T. (1989). Non-invasive image analysis evaluation of growth during plant micropropagation. Plant Cell, Tissue and Organ Culture, 189, 91–102.

    Article  Google Scholar 

  • Somerville, C., & Briscoe, L. (2001). Genetic engineering and water. Science, 292, 2217.

    Article  CAS  PubMed  Google Scholar 

  • Sozzani, R., Busch, W., Spalding, E. P., & Benfey, P. N. (2014). Advanced imaging techniques for the study of plant growth and development. Trends in Plant Science, 19(5), 304–310.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stirbet, A., & Govindjee (2011). On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: basics and applications of the OJIP fluorescence transient. Journal of Photochemistry and Photobiology B: Biology, 104, 236–257. doi:10.1016/j.jphotobiol.2010.12.010.

    Article  CAS  Google Scholar 

  • Stober, F., Lang, M., & Lichtenthaler, H. K. (1994). Blue-green, and red fluorescence emission signatures of green etiolated and white leaves. Remote Sensing of Environment, 47(1), 65–71.

    Article  Google Scholar 

  • Svensgaard, J., Roitsch, T., & Christensen, S. (2014). Development of a mobile multispectral imaging platform for precise field phenotyping. Agronomy, 4, 322–336. doi:10.3390/agronomy4030322.

    Article  Google Scholar 

  • Sweeney, B. M., Prezelin, B. B., Wong, D., & Govindjee, (1979). In-vivo chlorophyll a fluorescence transients and the circadian rhythm of photosynthesis in Gonyaulax polyedra. Photochemical and Photobiology, 30, 309–311.

    Article  CAS  Google Scholar 

  • Thomson, J. A. (2002). Research needs to improve agricultural productivity and food quality, with emphasis on biotechnology. Journal of Nutrition, 132, 3441S–3442S.

    CAS  PubMed  Google Scholar 

  • Tikkanen, M., Grieco, M., Nurmi, M., Rantala, M., Suorsa, M., & Aro, E.-M. (2012). Regulation of the photosynthetic apparatus under fluctuating growth light. Philosophical Transactions of the Royal Society of London B Biological Sciences, 367, 3486–3493.

    Article  CAS  PubMed  Google Scholar 

  • Valliyodan, B., & Nguyen, H. T. (2006). Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Current Opinion of Plant Biology, 9, 189–195.

    Article  CAS  Google Scholar 

  • Walter, A., Liebisch, F., & Hund, A. (2015). Plant phenotyping: From bean weighing to image analysis. Plant Methods, 11, 14.

    Article  PubMed  PubMed Central  Google Scholar 

  • Walter, A., Scharr, H., Gilmer, F., Zierer, R., Nagel, K. A., Ernst, M., et al. (2007). Dynamics of seedling growth acclimation towards altered light conditions can be quantified via GROWSCREEN: A setup and procedure designed for rapid optical phenotyping of different plant species. New Phytologist, 174, 447–455.

    Article  PubMed  Google Scholar 

  • Walter, T., Shattuck, D. W., Baldock, R., Bastin, M. E., Carpenter, A. E., Duce, S., et al. (2010). Visualization of image data from cells to organisms. Nature Methods, 7, S26–S41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wan, S., & Jiang, L. (2016). Endoplasmic reticulum (ER) stress and the unfolded protein response (UPR) in plants. Protoplasma, 253, 753–764.

    Article  CAS  PubMed  Google Scholar 

  • Wang, J. B., Guo, Y. L., Ding, B., Li, X., Liu, Y., & Xie, X. D. (2016). Screening of stomatal mutants in Arabidopsis using a novel controlled environmental infrared imaging system. Plant Growth Regulation, 79(2), 157–165.

    Article  CAS  Google Scholar 

  • Wasson, A. P., Bischof, L., Zwart, A., & Watt, M. (2016). A portable fluorescence spectroscopy imaging system for automated root phenotyping in soil cores in the field. Journal of Experimental Botany, 67, 1033–1043.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woo, N. S., Badger, M. R., & Pogson, B. J. (2008). A rapid, non-invasive procedure for quantitative assessment of drought survival using chlorophyll fluorescence. Plant Methods, 27, 4.

    Google Scholar 

  • Zenone, T., Morelli, G., Teobaldelli, M., Fischanger, F., Matteucci, M., et al. (2008). Preliminary use of ground-penetrating radar and electrical resistivity tomography to study tree roots in pine forests and poplar plantations. Functional Plant Biology, 35, 1047–1058.

    Article  Google Scholar 

  • Zhang, C., & Kovacs, J. M. (2012). The application of small unmanned aerial systems for precision agriculture: A review. Precision Agriculture, 13, 693–712.

    Article  CAS  Google Scholar 

  • Zhong, D., Bohn, M., Han, J., Novais, J., & Grift, T. E. (2009). Maize root complexity analysis using a Support Vector Machine method. Computer and Electronics in Agriculture, 69, 46–50.

    Article  Google Scholar 

  • Zhu, J., Ingram, P. A., Benfey, P. N., & Elich, T. (2011). From lab to field, new approaches to phenotyping root system architecture. Current Opinion in Plant Biology, 14, 310–317.

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank the Ministry of Education, Youth and Sports within the National Programme for Sustainability (Grant No. LO1415), and the Czech Science Foundation (Project No. 13-28093S). AM thanks internal postdoctoral project from the Czech Academy of Sciences for the support. Govindjee thanks all the staff of Information Technology, Life Sciences; the offices of the Department of Plant Biology, of the Department of Biochemistry, and of the Center of Biophysics and Quantitative Biology, University of Illinois at Urbana-Champaign, for their help. We thank David Kramer and Jeff Cruz (Michigan State University, USA) for their valuable suggestions during the preparation of this review.

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  1. Global Change Research Institute, The Czech Academy of Sciences, Bělidla 986/4a, 603 00, Brno, Czech Republic

    Kumud B. Mishra, Anamika Mishra & Karel Klem

  2. Department of Plant Biology, Department of Biochemistry and Center for Biophysics and Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA

    Govindjee

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Mishra, K.B., Mishra, A., Klem, K. et al. Plant phenotyping: a perspective. Ind J Plant Physiol. 21, 514–527 (2016). https://doi.org/10.1007/s40502-016-0271-y

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