Combining IR imaging, chlorophyll fluorescence and phenomic approach for assessing diurnal canopy temperature dynamics and desiccation stress management in Azadirachta indica and Terminalia mantaly

  • Sukumar TariaEmail author
  • Jagadish Rane
  • Badre Alam
  • Mahesh Kumar
  • Rohit Babar
  • Hirdayesh Anuragi
  • K. Rajarajan
  • Narendra Pratap Singh


Infrared (IR) imaging, chlorophyll fluorescence imaging and plant phenomic approach were used to study physiological mechanism of desiccation tolerance in Azadirachta indica and Terminalia mantaly during the period of November 2018 to February 2019. IR imaging instrument was installed in the field for monitoring the canopy temperature dynamics of different canopy level including stem region of the tree throughout the day. Maximum photochemical efficiency (Fv/Fm) was measured with chlorophyll fluorescence measuring system for sun exposed leaves of A. indica and T. mantaly over a period of desiccation. In order to reveal complete understanding of physiological mechanism of desiccation tolerance, plant phenomic approach was used for assessing response of these tree species to exposed desiccation. Results indicated that canopy temperature of upper foliage, lower foliage, stem (trunk) region of A. indica were quite higher during the hotter period of the day as compared to T. mantaly and maximum photochemical efficiency (Fv/Fm) was maintained in A. indica leaves as compared to T. mantaly for same exposed duration of desiccation. Plant phenomic approach also depicted that A. indica twig retained more tissue water and maintained canopy volume area higher than T. mantaly. Thus it provides an indication that A. indica tree is quite desiccation tolerant than T. mantaly by maintaining its canopy temperature, maximum photochemical efficiency, more tissue water and canopy area.


Azadirachta indica Terminalia mantaly IR imaging Chlorophyll fluorescence Plant phenomic 



The authors gratefully acknowledge Indian council of Agricultural Research and ICAR-Central Agroforestry Research Institute, Jhansi for facilitating three months professional attachment training program at ICAR- National Institute of Abiotic Stress Management, Baramati. The authors also acknowledge facilities including phenomic platform provided for this work at ICAR-National Institute of Abiotic Stress Management, Baramati.


  1. Ahmed S, Nawata E, Hosokawa M, Domae Y, Sakuratani T (2002) Alterations in photosynthesis and some antioxidant enzymatic activities of mung bean subjected to water logging. Plant Sci 163:117–123CrossRefGoogle Scholar
  2. Alam B, Nair DB, Jacob J (2005) Low temperature stress modifies the photochemical efficiency of a tropical tree species Hevea brasiliensis: effects of varying levels of CO2 and photon flux density. Photosynthetica 43(2):247–252CrossRefGoogle Scholar
  3. Alam B, Jacob J, Earl HJ (2010) Photosynthetic efficiency of transgenic tobacco plants (Nicotiana tabacum L.) over-expressing mtlD gene under drought and paraquat stress. Indian J Plant Physiol 15(2):186–191Google Scholar
  4. Amani I, Fischer RA, Reynolds MP (1996) Canopy temperature depression association with yield of irrigated spring wheat cultivars in hot climate. J Agron Crop Sci 176:119–129CrossRefGoogle Scholar
  5. Anjum SA, Wang LC, Farooq M, Hussain M, Xue LL, Zou CM (2011) Brassinolide application improves the Drought tolerance in maize through modulation of enzymatic antioxidants and leaf gas exchange. J Agron Crop Sci 197:177–185. CrossRefGoogle Scholar
  6. Barnabas B, Jäger K, Fehér A (2008) The effect of Drought and heat stress on reproductive processes in cereals. Plant Cell Environ 31:11–38PubMedGoogle Scholar
  7. Berger S, Benediktyova Z, Matous K, Benfig K, Mueller MJ, Medbal L, Roitsch T (2007) Visualization of dynamics of plant– pathogen interaction by novel combination of chlorophyll fluorescence imaging and statistical analysis: differential effects of virulent and a virulent strains of P. syringae and of oxylipins on A. thaliana. J Exp Bot 58:797–806CrossRefPubMedGoogle Scholar
  8. Berger B, Parent B, Tester M (2010) High throughput shoot imaging to study Drought responses. J Exp Bot 61:3519–3528CrossRefPubMedGoogle Scholar
  9. Blödner C, Skroppa T, Johnson O, Polle A (2005) Freezing tolerance in two Norway spruce (Picea abies [L.] Karst.) progenies is physiologically correlated with Drought tolerance. Plant Physiol 162:549–558CrossRefGoogle Scholar
  10. Blom-Zandstra M, Metselaar K (2006) Infrared thermometry for early detection of Drought stress in Chrysanthemum. HortScience 41:136–142CrossRefGoogle Scholar
  11. Blum A, Shipiler L, Golan G, Mayer J (1989) Yield stability and canopy temperature of wheat genotypes under Drought stress. Field Crops Res 22:289–296CrossRefGoogle Scholar
  12. Boyer JS (1970) Differing sensitivity of photosynthesis to low leaf water potentials in corn and soybean. Plant Physiol 46:236–239CrossRefPubMedPubMedCentralGoogle Scholar
  13. Cen H, Weng H, Yao J, He M, Lv J, Hua S et al (2017) Chlorophyll fluorescence imaging uncovers photosynthetic fingerprint of citrus Huanglongbing. Front Plant Sci 8:1509. CrossRefPubMedPubMedCentralGoogle Scholar
  14. Chaerle L, Van Der Straeten D (2000) Imaging techniques and the early detection of plant stress. Trends Plant Sci 5:495–501CrossRefPubMedGoogle Scholar
  15. Chaerle L, Van Der Straeten D (2001) Seeing is believing: imaging techniques to monitor plant health. Biochim Biophys Acta 1519:153–166CrossRefPubMedGoogle Scholar
  16. Chrispeels MJ, Sadava DE (2003) Plants, genes, and crop biotechnology. Jones and Bartlett, BostonGoogle Scholar
  17. De Bei R, Cozzolino D, Sullivan W, Cynkar W, Fuentes S, Dambergs R, Pech J, Tyerman S (2011) Nondestructive measurement of grapevine water potential using near infrared spectroscopy. Aust J Grape Wine Res 17:62–71CrossRefGoogle Scholar
  18. Duan L, Huang C, Chen G, Xiong L, Liu Q, Yang W (2015) Determination of rice panicle numbers during heading by multi-angle imaging. Crop J 3:211–219. CrossRefGoogle Scholar
  19. Eitel JUH, Gessler PE, Smith AMS, Robberecht R (2006) Suitability of existing and novel spectral indices to remotely detect water stress in Populus spp. For Ecol Manag 229:170–182CrossRefGoogle Scholar
  20. European Environment Agency (2004) Impacts of Europe’s changing climate. EEA report no. 2/2004Google Scholar
  21. Finkel E (2009) With ‘phenomic’ plant scientists hope to shift breeding into overdrive. Science 325:380–381CrossRefPubMedGoogle Scholar
  22. Furbank RT, Von Caemmerer S, Sheehy J, Edwards G (2009) C4 rice: a challenge for plant phenomic. Funct Plant Biol 36:845–856CrossRefGoogle Scholar
  23. Galle A, Csiszar J, Tari I, Erdei L (2002) Changes in water and chlorophyll fluorescence parameters under osmotic stress in wheat cultivars. Acta Biol Szeged 46(3–4):85–86Google Scholar
  24. Gielen B, De Boeck HJ, Lemmens CMHM, Valcke R, Nijs I, Ceulemans R (2005) Grassland species will not necessarily benefit from future elevated air temperatures: a chlorophyll fluorescence approach to study autumn physiology. Physiol Plant 125:52–63CrossRefGoogle Scholar
  25. Granier C, Aguirrezabal L, Chenu K 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 Phytol 169:623–635CrossRefPubMedGoogle Scholar
  26. Haddy A (2007) EPR spectroscopy of the manganese cluster of photosystem II. Photosynth Res 92:357–368CrossRefPubMedGoogle Scholar
  27. Hamanishi ET, Campbell MM (2011) Genome-wide responses to Drought in forest trees. Forestry 84:273–283. CrossRefGoogle Scholar
  28. Hatfield JL, Quisenberry JE, Dilbeck RE (1987) Use of canopy temperatures to identify water conservation in cotton germplasm. Crop Sci 27:269–273CrossRefGoogle Scholar
  29. Horie T, Matsuura S, Takai T, Kuwasaki K, Ohsumi A, Shiraiwa T (2006) Genotypic difference in canopy diffusive conductance measured by a new remote-sensing method and its association with the difference in rice yield potential. Plant Cell Environ 29:653–660CrossRefPubMedGoogle Scholar
  30. Houghton JT, Ding Y, Griggs DJ, Noguer M, Van der Linden PJ, Dai X, Maskell K, Johnson CA (2001) Climate change 2001: the scientific basis. Cambridge University Press, CambridgeGoogle Scholar
  31. Humplik JF, Lazar D, Furst T, Husickova A, Hybl M, Spichal L (2015) Automated integrative high-throughput phenotyping of plant shoots: a case study of the cold-tolerance of pea (Pisum sativum L.). Plant Methods 11:20. CrossRefPubMedPubMedCentralGoogle Scholar
  32. Jansen M, Gilmer F, Biskup B, Nagel K, 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. Funct Plant Biol 36:902–914CrossRefGoogle Scholar
  33. Jones HG (2004) Application of thermal imaging and infrared sensing in plant physiology and ecophysiology. Adv Bot Res Inc Adv Plant Pathol 41:107–163CrossRefGoogle Scholar
  34. Jones HG, Stoll M, Santos T, Sousa CD, Chaves MM, Grant OM (2002) Use of infrared thermography for monitoring stomatal closure in the field: application to grapevine. J Exp Biol 53:2249–2260Google Scholar
  35. Kawakami K, Umenab Y, Kamiyab N, Shen J (2009) Location of chloride and its possible functions in oxygen-evolving photosystem II revealed by X-ray crystallography. Proc Natl Acad Sci USA 106:8567–8572CrossRefPubMedGoogle Scholar
  36. Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349CrossRefGoogle Scholar
  37. Kumari N, Sharma V (2010) Stress-mediated alteration in V-ATPase and V-PPase of Butea monosperma. Protoplasma 245:125CrossRefPubMedGoogle Scholar
  38. Kümmerlen B, Dauwe S, Schmundt D, Schurr U (1999) Thermography to measure water relations of plant leaves. In: Jähne B, Haußecker H, Geißler P (eds) Handbook of computer vision and applications. Vol 3. Systems and applications. Academic Press, Boston, pp 763–781Google Scholar
  39. Lichtenthaler HK, MieheJ A (1997) Fluorescence imaging as a diagnostic tool for plant stress. Trends Plant Sci 2:316–320CrossRefGoogle Scholar
  40. Lobell DB, Schlenker W, Costa-Roberts J (2011) Climate trends and global crop production since 1980. Science 333:616–620. CrossRefPubMedPubMedCentralGoogle Scholar
  41. Lu Q, Lu C, Zhang J, Kuang T (2002) Photosynthesis and chlorophyll a fluorescence during flag leaf senescence of filed grown wheat plants. J Plant Physiol 159:1173–1178CrossRefGoogle Scholar
  42. Montagnoli A, Terzaghi M, Fulgaro N, Stoew B, Wipenmyr J, Ilver D et al (2016) Non-destructive phenotypic analysis of early stage tree seedling growth using an automated stereovision imaging method. Front Plant Sci 7:1644. CrossRefPubMedPubMedCentralGoogle Scholar
  43. Monteith JL (1977) Climate and efficiency of crop production in Britain. Philos Trans R Soc Lond Ser B Biol Sci 281:277–294CrossRefGoogle Scholar
  44. Nilsson HE (1995) Remote sensing and image analysis in plant pathology. Annu Rev Phytopathol 33:489–527CrossRefPubMedGoogle Scholar
  45. Oerke EC, Dehne HW (2004) Safeguarding production—losses in major crops and the role of crop protection. Crop Prot 23:275–285CrossRefGoogle Scholar
  46. Omasa K, Takayama K (2003) Simultaneous measurement of stomatal conductance, non-photochemical quenching, and photochemical yield of photosystem II in intact leaves by thermal and chlorophyll fluorescence imaging. Plant Cell Physiol 44:1290–1300CrossRefPubMedGoogle Scholar
  47. Petrozza A, Santaniello A, Summerer S, Di Tommaso G, Di Tommaso D, Paparelli E et al (2014) Physiological responses to megafol (R) treatments in tomato plants under Drought stress: a phenomic and molecular approach. Sci Hortic 174:185–192. CrossRefGoogle Scholar
  48. Pineda M, Gaspar L, Morales F, Szigeti Z, Baron M (2008) Multicolor fluorescence imaging of leaves—a useful tool for visualizing systemic viral infections in plants. Photochem Photobiol 84:1048–1060. CrossRefPubMedGoogle Scholar
  49. Qiu GY, Omasa K, Sase S (2009) An infrared-based coefficient to screen plant environmental stress: concept, test and applications. Funct Plant Biol 36:990–997CrossRefGoogle Scholar
  50. Rajendran K, Tester M, Roy SJ (2009) Quantifying the three main components of salinity tolerance in cereals. Plant Cell Environ 32:237–249CrossRefPubMedGoogle Scholar
  51. Rebolledo MC, Peña AL, Duitama J, Cruz DF, Dingkuhn M, Grenier C et al (2016) Combining image analysis, genome wide association studies and different field trials to reveal stable genetic regions related to panicle architecture and the number of spikelets per panicle in rice. Front Plant Sci 7:1384. CrossRefPubMedPubMedCentralGoogle Scholar
  52. Renger G (2001) Photosynthetic water oxidation to molecular oxygen: apparatus and mechanism. Biochim Biophys Acta 1503:210–228CrossRefPubMedGoogle Scholar
  53. Rolfe SA, Scholes JD (1995) Quantitative imaging of chlorophyll fluorescence. New Phytol 131:69–79CrossRefGoogle Scholar
  54. Saab IN, Sharp RE (1989) Non-hydraulic signals from maize roots in drying soil: inhibition of leaf elongation but not stomatal conductance. Planta 179:466–474CrossRefPubMedGoogle Scholar
  55. Schuppler U, He PH, John PCL, Munns R (1998) Effects of water stress on cell division and cell-division-cycle-2-like cell-cycle kinase activity in wheat leaves. Plant Physiol 117:667–678CrossRefPubMedPubMedCentralGoogle Scholar
  56. Seelig HD, Hoehn A, Stodieck LS, Klaus DM, Adams WW, Emery WJ (2008) The assessment of leaf water content using leaf reflectance ratios in the visible, near-, and short-wave-infrared. Int J Remote Sens 29:3701–3713CrossRefGoogle Scholar
  57. Shao G, Huang D, Cheng X, Cui J, Zhang Z (2016) Path analysis of sap flow of tomato under rain shelters in response to Drought stress. Int J Agric Biol Eng 9(2):54–62Google Scholar
  58. Soukupova J, Smatanova S, Nedbal L, Jegorov A (2003) Plant response to destruxins visualized by imaging of chlorophyll fluorescence. Physiol Plant 118:399–405CrossRefGoogle Scholar
  59. Spalding EP, Miller ND (2013) Image analysis is driving a renaissance in growth measurement. Curr Opin Plant Biol 16:100–104. CrossRefPubMedGoogle Scholar
  60. Stark JC, Pavek JJ (1987) Selection of Drought tolerant potato clones using foliage temperature measurements. In: 10th Triennial Conf. Eur. Assn. Potato Res., pp 26–27 (Abstr.)Google Scholar
  61. Tackenberg O (2007) A new method for non-destructive measurement of biomass, growth rates, vertical biomass distribution and dry matter content based on digital image analysis. Ann Bot 99:777–783CrossRefPubMedPubMedCentralGoogle Scholar
  62. Turner NC, Wright GC, Siddique KHM (2001) Adaptation of grain legumes (pulses) to water-limited environments. Adv Agron 71:193–231. CrossRefGoogle Scholar
  63. Verhoef A (2004) Remote estimation of thermal inertia and soil heat flux for bare soil. Agric For Meteorol 123:221–236CrossRefGoogle Scholar
  64. Verstraeten WW, Veroustraete F, Van der Sande CJ, Grootaers L, Feyen J (2006) Soil moisture retrieval using thermal inertia, determined with visible and thermal space borne data, validated for European forests. Remote Sens Environ 101:299–314CrossRefGoogle Scholar
  65. Wedeking R, Mahlein AK, Steiner U, Oerke EC, Goldbach HE, Wimmer MA (2017) Osmotic adjustment of young sugar beets (Beta vulgaris) under progressive Drought stress and subsequent rewatering assessed by metabolite analysis and infrared thermography. Funct Plant Biol 44:119–133CrossRefGoogle Scholar
  66. West JD, Peak D, Peterson JQ, Mott KA (2005) Dynamics of stomatal patches for a single surface of Xanthium strumarium L. leaves observed with fluorescence and thermal images. Plant Cell Environ 28:633–641CrossRefGoogle Scholar
  67. Wiese A, Christ MM, Virnich O, Schurr U, Walter A (2007) Spatiotemporal leaf growth patterns of Arabidopsis thaliana and evidence for sugar control of the diel leaf growth cycle. New Phytol 174:752–761CrossRefPubMedGoogle Scholar
  68. Yordanov I, Velikova V, Tsonev T (2000) Plant responses to Drought, acclimation, and stress tolerance. Photosynthetica 38:171–186. CrossRefGoogle Scholar
  69. Zlatve ZS, Yordanov IT (2004) Effects of soil Drought on photosynthesis and chlorophyll fluorescence in bean plants. Bulg J Plant Physiol 30:3–18Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.ICAR-Central Agroforestry Research InstituteJhansiIndia
  2. 2.ICAR-National Institute of Abiotic Stress ManagementBaramatiIndia

Personalised recommendations