Distinct growth and physiological responses of Arabidopsis thaliana natural accessions to drought stress and their detection using spectral reflectance and thermal imaging
Karel Klem A C , Kumud B. Mishra A , Kateřina Novotná A B , Barbora Rapantová A B , Petra Hodaňová A B , Anamika Mishra A , Daniel Kováč A and Otmar Urban A
+ Author Affiliations
- Author Affiliations
A Global Change Research Institute CAS, Bělidla 986/4a, 603 00 Brno, Czech Republic.
B Mendel University in Brno, Zemědělská 1, 613 00 Brno, Czech Republic.
C Corresponding author. Email: klem.k@czechglobe.cz
Functional Plant Biology 44(3) 312-323 https://doi.org/10.1071/FP16194
Submitted: 24 May 2016 Accepted: 5 November 2016 Published: 16 December 2016
Abstract
Reduced growth and stomatal closure are the two main responses of plants to drought stress. The extent to which these processes are connected and whether different genotypes prefer one over the other remains unclear. To understand the genotype-specific interconnections of these two processes and evaluate potential utilisation of this knowledge for drought tolerance phenotyping, six natural accessions of Arabidopsis thaliana (L.) Heynh. were exposed to drought stress for 10 days. Projected leaf area of rosette, light-saturated CO2 assimilation rate (Amax), relative water content (RWC), leaf temperature (thermal imaging), and spectral reflectance were measured through the course of induced drought stress. Three types of acclimation were identified: (i) growth not affected but Amax significantly reduced, (ii) both growth and Amax significantly reduced, and (iii) growth significantly reduced but only small decrease in Amax. Within the last type, the smallest decline in RWC was evident. These results show that a substantial reduction in leaf area may cause a decline in transpiration that enables maintenance of both RWC and physiological processes. Both non-invasive thermal imaging and spectral reflectance measurements proved reliable tools for tracking drought-induced changes in Amax and RWC across all accessions tested and thus are effective tools for phenotyping stress tolerance.
Additional keywords: drought tolerance, genotypic variation, leaf water status, photosynthesis, plant phenomics.
References
Anyia AO, Herzog H (2004) Genotypic variability in drought performance and recovery in cowpea under controlled environment. Journal of Agronomy & Crop Science 190, 151–159.| Genotypic variability in drought performance and recovery in cowpea under controlled environment.Crossref | GoogleScholarGoogle Scholar |
Aparicio N, Villegas D, Casadesus J, Araus JL, Royo C (2000) Spectral vegetation indices as nondestructive tools for determining durum wheat yield. Agronomy Journal 92, 83–91.
| Spectral vegetation indices as nondestructive tools for determining durum wheat yield.Crossref | GoogleScholarGoogle Scholar |
Berger B, Parent B, Tester M (2010) High-throughput shoot imaging to study drought responses. Journal of Experimental Botany 61, 3519–3528.
| High-throughput shoot imaging to study drought responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVert7vO&md5=e657e2d8437099f764718b85f3a9d92aCAS |
Blum A (2005) Drought resistance, water-use efficiency, and yield potential – are they compatible, dissonant, or mutually exclusive? Crop & Pasture Science 56, 1159–1168.
| Drought resistance, water-use efficiency, and yield potential – are they compatible, dissonant, or mutually exclusive?Crossref | GoogleScholarGoogle Scholar |
Blum A (2009) Effective use of water (EUW) and not water-use efficiency (WUE) is the target of crop yield improvement under drought stress. Field Crops Research 112, 119–123.
| Effective use of water (EUW) and not water-use efficiency (WUE) is the target of crop yield improvement under drought stress.Crossref | GoogleScholarGoogle Scholar |
Bouchabke O, Chang F, Simon M, Voisin R, Pelletier G, Durand-Tardif M (2008) Natural variation in Arabidopsis thaliana as a tool for highlighting differential drought responses. PLoS One 3, e1705
| Natural variation in Arabidopsis thaliana as a tool for highlighting differential drought responses.Crossref | GoogleScholarGoogle Scholar |
Boyer JS, James RA, Munns R, Condon TG, Passioura JB (2008) Osmotic adjustment leads to anomalously low estimates of relative water content in wheat and barley. Functional Plant Biology 35, 1172–1182.
| Osmotic adjustment leads to anomalously low estimates of relative water content in wheat and barley.Crossref | GoogleScholarGoogle Scholar |
Cornic G (2000) Drought stress inhibits photosynthesis by decreasing stomatal aperture–not by affecting ATP synthesis. Trends in Plant Science 5, 187–188.
| Drought stress inhibits photosynthesis by decreasing stomatal aperture–not by affecting ATP synthesis.Crossref | GoogleScholarGoogle Scholar |
Fatichi S, Leuzinger S, Körner C (2014) Moving beyond photosynthesis: from carbon source to sink‐driven vegetation modeling. New Phytologist 201, 1086–1095.
| Moving beyond photosynthesis: from carbon source to sink‐driven vegetation modeling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitVegs7s%3D&md5=504eda6bfdc0896f0696f47b5128633aCAS |
Flexas J, Medrano H (2002) Drought‐inhibition of photosynthesis in C3 plants: stomatal and non‐stomatal limitations revisited. Annals of Botany 89, 183–189.
| Drought‐inhibition of photosynthesis in C3 plants: stomatal and non‐stomatal limitations revisited.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkslymsLs%3D&md5=23430a053c49ba567760cc7a92fde2daCAS |
Flexas J, Bota J, Loreto F, Cornic G, Sharkey TD (2004) Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biology 6, 269–279.
| Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c3ksVOlug%3D%3D&md5=b4062b257bc77b66ab158f9ee66c1371CAS |
Furbank RT, Tester M (2011) Phenomics – technologies to relieve the phenotyping bottleneck. Trends in Plant Science 16, 635–644.
| Phenomics – technologies to relieve the phenotyping bottleneck.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFOhu7%2FJ&md5=b61a1e3f534159863d82ad6b44ce19fdCAS |
Granier C, Aguirrezabal L, Chenu K, Cookson SJ, Dauzat M, Hamard P, Thioux JJ, Rolland G, Bouchier-Combaud S, Lebaudy A, Muller B, Simonneau T, Tardieu F (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.
| 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.Crossref | GoogleScholarGoogle Scholar |
Grumet R, Albrechtsen RS, Hanson AD (1987) Growth and yield of barley isopopulations differing in solute potential. Crop Science 27, 991–995.
| Growth and yield of barley isopopulations differing in solute potential.Crossref | GoogleScholarGoogle Scholar |
Gutierrez M, Reynolds MP, Klatt AR (2010) Association of water spectral indices with plant and soil water relations in contrasting wheat genotypes. Journal of Experimental Botany 61, 3291–3303.
| Association of water spectral indices with plant and soil water relations in contrasting wheat genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXptVymsL4%3D&md5=347bc65bbce17c642e0adbdc136e007bCAS |
Hatfield JL, Gitelson AA, Schepers JS, Walthall CL (2008) Application of spectral remote sensing for agronomic decisions. Agronomy Journal 100, S-117–S-131.
| Application of spectral remote sensing for agronomic decisions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnsFGitbo%3D&md5=eaf536f658b0039e818c72864b10ad42CAS |
Jackson RD, Idso SB, Reginato RJ, Pinter PJ (1981) Canopy temperature as a crop water stress indicator. Water Resources Research 17, 1133–1138.
| Canopy temperature as a crop water stress indicator.Crossref | GoogleScholarGoogle Scholar |
Jones HG (1998) Stomatal control of photosynthesis and transpiration. Journal of Experimental Botany 49, 387–398.
| Stomatal control of photosynthesis and transpiration.Crossref | GoogleScholarGoogle Scholar |
Jones HG, Serraj R, Loveys BR, Xiong L, Wheaton A, Price AH (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.
| Thermal infrared imaging of crop canopies for the remote diagnosis and quantification of plant responses to water stress in the field.Crossref | GoogleScholarGoogle Scholar |
Körner C (2003) Carbon limitation in trees. Journal of Ecology 91, 4–17.
| Carbon limitation in trees.Crossref | GoogleScholarGoogle Scholar |
Lecoeur J, Wery J, Turc O (1992) Osmotic adjustment as a mechanism of dehydration postponement in chickpea (Cicer arietinum L.) leaves. Plant and Soil 144, 177–189.
| Osmotic adjustment as a mechanism of dehydration postponement in chickpea (Cicer arietinum L.) leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XmtV2jurc%3D&md5=d5902350a3248d667025a194de886f66CAS |
Levitt J (1972) Water deficit (or drought) stress. In ‘Responses of plants to environmental stresses’. (Ed. J Levitt) pp. 322–352. (Academic Press: New York)
Lobell DB, Schlenker W, Costa-Roberts J (2011) Climate trends and global crop production since 1980. Science 333, 616–620.
| Climate trends and global crop production since 1980.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpt1yisLs%3D&md5=5b821e31e79df53d0ae0982a2b3b9375CAS |
Matin MA, Brown JH, Ferguson H (1989) Leaf water potential, relative water content, and diffusive resistance as screening techniques for drought resistance in barley. Agronomy Journal 81, 100–105.
| Leaf water potential, relative water content, and diffusive resistance as screening techniques for drought resistance in barley.Crossref | GoogleScholarGoogle Scholar |
Meehl GA, Stocker TF, Collins WD, Friedlingstein P, Gaye AT, Gregory JM, Kitoh A, Knutti R, Murphy JM, Noda A, Raper SCB, Watterson IG, Weaver AJ, Zhao ZC (2007) Global climate projections. In ‘Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change’. (Eds S Solomon, D Qin, M Manning, Z Chen, M Marquis, KB Averyt, M Tignor, HL Miller) pp. 747–845. (Cambridge University Press: Cambridge, UK)
Merlot S, Mustilli AC, Genty B, North H, Lefebvre V, Sotta B, Vavasseur A, Giraudat J (2002) Use of infrared thermal imaging to isolate Arabidopsis mutants defective in stomatal regulation. The Plant Journal 30, 601–609.
| Use of infrared thermal imaging to isolate Arabidopsis mutants defective in stomatal regulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsFyktLc%3D&md5=b118ca38cc4b3ac6796f8c4708712fd4CAS |
Mitchell JH, Siamhan D, Wamala MH, Risimeri JB, Chinyamakobvu E, Henderson SA, Fukai S (1998) The use of seedling leaf death score for evaluation of drought resistance of rice. Field Crops Research 55, 129–139.
| The use of seedling leaf death score for evaluation of drought resistance of rice.Crossref | GoogleScholarGoogle Scholar |
Nikinmaa E, Hölttä T, Hari P, Kolari P, Mäkelä A, Sevanto S, Vesala T (2013) Assimilate transport in phloem sets conditions for leaf gas exchange. Plant, Cell & Environment 36, 655–669.
| Assimilate transport in phloem sets conditions for leaf gas exchange.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1ais74%3D&md5=56c526fd1fa3e942620e7e749240b4acCAS |
Nir I, Moshelion M, Weiss D (2014) The Arabidopsis GIBBERELLIN METHYL TRANSFERASE 1 suppresses gibberellin activity, reduces whole‐plant transpiration and promotes drought tolerance in transgenic tomato. Plant, Cell & Environment 37, 113–123.
| The Arabidopsis GIBBERELLIN METHYL TRANSFERASE 1 suppresses gibberellin activity, reduces whole‐plant transpiration and promotes drought tolerance in transgenic tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVyjurbK&md5=03081632d8cefbc8307398c00d565f51CAS |
Prashar A, Jones HG (2014) Infra-red thermography as a high-throughput tool for field phenotyping. Agronomy 4, 397–417.
| Infra-red thermography as a high-throughput tool for field phenotyping.Crossref | GoogleScholarGoogle Scholar |
Ritchie SW, Nguyen HT, Holaday AS (1990) Leaf water content and gas-exchange parameters of two wheat genotypes differing in drought resistance. Crop Science 30, 105–111.
| Leaf water content and gas-exchange parameters of two wheat genotypes differing in drought resistance.Crossref | GoogleScholarGoogle Scholar |
Salekdeh GH, Reynolds M, Bennett J, Boyer J (2009) Conceptual framework for drought phenotyping during molecular breeding. Trends in Plant Science 14, 488–496.
| Conceptual framework for drought phenotyping during molecular breeding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtV2lurnK&md5=99c8eee6d359e16f86f3589f42652c7eCAS |
Schlemmer MR, Francis DD, Shanahan JF, Schepers JS (2005) Remotely measuring chlorophyll content in corn leaves with differing nitrogen levels and relative water content. Agronomy Journal 97, 106–112.
| Remotely measuring chlorophyll content in corn leaves with differing nitrogen levels and relative water content.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhs1CjtL4%3D&md5=fdc6fc479ac337fa2baf286f5459fa85CAS |
Schonfeld MA, Johnson RC, Carver BF, Mornhinweg DW (1988) Water relations in winter wheat as drought resistance indicators. Crop Science 28, 526–531.
| Water relations in winter wheat as drought resistance indicators.Crossref | GoogleScholarGoogle Scholar |
Seelig HD, Hoehn A, Stodieck LS, Klaus DM, Adams WW, Emery WJ (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, 357–365.
| Plant water parameters and the remote sensing R 1300/R 1450 leaf water index: controlled condition dynamics during the development of water deficit stress.Crossref | GoogleScholarGoogle Scholar |
Tardieu F, Granier C, Muller B (2011) Water deficit and growth. Co-ordinating processes without an orchestrator? Current Opinion in Plant Biology 14, 283–289.
| Water deficit and growth. Co-ordinating processes without an orchestrator?Crossref | GoogleScholarGoogle Scholar |
Teulat B, Rekika D, Nachit MM, Monneveux P (1997) Comparative osmotic adjustments in barley and tetraploid wheats. Plant Breeding 116, 519–523.
| Comparative osmotic adjustments in barley and tetraploid wheats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnvFOrsw%3D%3D&md5=62109e1001442957bcfa65fd30476a0dCAS |
Tuberosa R (2012) Phenotyping for drought tolerance of crops in the genomics era. Frontiers in Physiology 3, 347
| Phenotyping for drought tolerance of crops in the genomics era.Crossref | GoogleScholarGoogle Scholar |
Tuberosa R, Salvi S (2006) Genomics-based approaches to improve drought tolerance of crops. Trends in Plant Science 11, 405–412.
| Genomics-based approaches to improve drought tolerance of crops.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xns1KjurY%3D&md5=a98a657bd352664df3496839297910ecCAS |
Türkan İ, Bor M, Özdemir F, Koca H (2005) Differential responses of lipid peroxidation and antioxidants in the leaves of drought-tolerant P. acutifolius Gray and drought-sensitive P. vulgaris L. subjected to polyethylene glycol mediated water stress. Plant Science 168, 223–231.
| Differential responses of lipid peroxidation and antioxidants in the leaves of drought-tolerant P. acutifolius Gray and drought-sensitive P. vulgaris L. subjected to polyethylene glycol mediated water stress.Crossref | GoogleScholarGoogle Scholar |
Weber VS, Araus JL, Cairns JE, Sanchez C, Melchinger AE, Orsini E (2012) Prediction of grain yield using reflectance spectra of canopy and leaves in maize plants grown under different water regimes. Field Crops Research 128, 82–90.
| Prediction of grain yield using reflectance spectra of canopy and leaves in maize plants grown under different water regimes.Crossref | GoogleScholarGoogle Scholar |
Wright GC, Nageswara Rao RC, Farquhar GD (1994) Water-use efficiency and carbon isotope discrimination in peanut under water deficit conditions. Crop Science 34, 92–97.
| Water-use efficiency and carbon isotope discrimination in peanut under water deficit conditions.Crossref | GoogleScholarGoogle Scholar |
Wright PR, Morgan JM, Jessop RS (1996) Comparative adaptation of canola (Brassica napus) and Indian mustard (B. juncea) to soil water deficits: plant water relations and growth. Field Crops Research 49, 51–64.
| Comparative adaptation of canola (Brassica napus) and Indian mustard (B. juncea) to soil water deficits: plant water relations and growth.Crossref | GoogleScholarGoogle Scholar |
Zarco-Tejada PJ, Miller JR, Noland TL, Mohammed GH, Sampson PH (2001) Scaling-up and model inversion methods with narrowband optical indices for chlorophyll content estimation in closed forest canopies with hyperspectral data. IEEE Transactions on Geoscience and Remote Sensing 39, 1491–1507.
| Scaling-up and model inversion methods with narrowband optical indices for chlorophyll content estimation in closed forest canopies with hyperspectral data.Crossref | GoogleScholarGoogle Scholar |
Zhang J, Davies WJ (1990) Does ABA in the xylem control the rate of leaf growth in soil-dried maize and sunflower plants? Journal of Experimental Botany 41, 1125–1132.
| Does ABA in the xylem control the rate of leaf growth in soil-dried maize and sunflower plants?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXlvVyhsLk%3D&md5=e1a417e7d58c8ea110296448cf78ffdbCAS |
