Abstract

Drought stress disrupts the balance of macro- and micronutrients and affects the yield of agriculturally and economically significant plants. Rapid detection of stress-induced changes of relative content of elements such as sodium (Na), potassium (K), calcium (Ca) and iron (Fe) in the field may allow farmers and crop growers to counter the effects of plant stress and to increase their crop return. Unfortunately, the analytical methods currently available are time-consuming, expensive and involve elaborate sample preparation such as acid digestion which hinders routine daily monitoring of crop health on a field scale. We report application of an alternative method for rapid detection of drought stress in plants using femtosecond laser-induced breakdown spectroscopy (LIBS). We demonstrate daily monitoring of relative content of Na, K, Ca and Fe in decorative indoor (gardenia) and cultivated outdoor (wheat) plant species under various degrees of drought stress. The observed differences in spectral and temporal responses indicate different mechanisms of drought resistance. We identify spectroscopic markers of drought stress which allow for distinguishing mild environmental and severe drought stress in wheat and may be used for remote field-scale estimation of plant stress resistance and health.

© 2017 Optical Society of America

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References

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2016 (1)

H. Chen, H. Li, Y. Sun, Y. Wang, and P. Lü, “Femtosecond laser for cavity preparation in enamel and dentin: ablation efficiency related factors,” Sci. Rep. 6(1), 20950 (2016).
[Crossref] [PubMed]

2015 (3)

K. Devey, M. Mucalo, G. Rajendram, and J. Lane, “Pasture vegetation elemental analysis by laser-induced breakdown spectroscopy,” Commun. Soil Sci. Plan. 46(S1), 72–80 (2015).
[Crossref]

G. G. de Carvalho, J. Moros, D. Santos, F. J. Krug, and J. J. Laserna, “Direct determination of the nutrient profile in plant materials by femtosecond laser-induced breakdown spectroscopy,” Anal. Chim. Acta 876, 26–38 (2015).
[Crossref] [PubMed]

R. Kanawade, F. Mahari, F. Klämpfl, M. Rohde, C. Knipfer, K. Tangermann-Gerk, W. Adler, M. Schmidt, and F. Stelzle, “Qualitative tissue differentiation by analysing the intensity ratios of atomic emission lines using laser induced breakdown spectroscopy (LIBS): prospects for a feedback mechanism for surgical laser systems,” J. Biophotonics 8(1-2), 153–161 (2015).
[Crossref] [PubMed]

2014 (6)

A. Porcar-Castell, E. Tyystjärvi, J. Atherton, C. van der Tol, J. Flexas, E. E. Pfündel, J. Moreno, C. Frankenberg, and J. A. Berry, “Linking chlorophyll a fluorescence to photosynthesis for remote sensing applications: mechanisms and challenges,” J. Exp. Bot. 65(15), 4065–4095 (2014).
[Crossref] [PubMed]

J. J. Casanova, S. A. O’Shaughnessy, S. R. Evett, and C. M. Rush, “Development of a wireless computer vision instrument to detect biotic stress in wheat,” Sensors (Basel) 14(9), 17753–17769 (2014).
[Crossref] [PubMed]

K. Hancke, B. K. Sorell, L. C. Lund-Hansen, M. Larsen, T. Hancke, and R. N. Glud, “Effects of temperature and irradiance on a benthic microalgal community: a combined two-dimensional oxygen and fluorescence imaging approach,” Limnol. Oceanogr. 59(5), 1599–1611 (2014).
[Crossref]

Z. Dong, X. Zhou, J. Wu, Z. Zhang, T. Li, Z. Zhou, S. Zhang, and G. Li, “Small incision lenticule extraction (SMILE) and femtosecond laser LASIK: comparison of corneal wound healing and inflammation,” Br. J. Ophthalmol. 98(2), 263–269 (2014).
[PubMed]

F. Chen and J. R. Vazquez de Aldana, “Optical waveguides in crystalline dielectric materials produced by femtosecond-laser micromachining,” Laser Photonics Rev. 8(2), 251–275 (2014).
[Crossref]

S. Zhang, X. Wang, M. He, Y. Jiang, B. Zhang, W. Hang, and B. Huang, “Laser-induced plasma temperature,” Spectrochim. Acta B At. Spectrosc. 97, 13–33 (2014).
[Crossref]

2013 (2)

A. A. Farjo, A. Sugar, S. C. Schallhorn, P. A. Majmudar, D. J. Tanzer, W. B. Trattler, J. B. Cason, K. E. Donaldson, and G. D. Kymionis, “Femtosecond lasers for LASIK flap creation: a report by the American Academy of Ophthalmology,” Ophthalmology 120(3), e5–e20 (2013).
[Crossref] [PubMed]

I. M. Ahmed, F. Cao, M. Zhang, X. Chen, G. Zhang, and F. Wu, “Difference in yield and physiological features in response to drought and salinity combined stress during anthesis in Tibetan wild and cultivated barleys,” PLoS One 8(10), e77869 (2013).
[Crossref] [PubMed]

2012 (5)

G. G. A. Carvalho, D. Santos, L. C. Nunes, M. S. Gomes, F. O. Leme, and F. J. Krug, “Effects of laser focusing and fluence on the analysis of pellets of plant materials by laser-induced breakdown spectroscopy,” Spectrochim. Acta B At. Spectrosc. 74–75, 162–168 (2012).

V. Vassileva, D. Demirevska, L. Simova-Stoilova, T. Petrova, N. Tsenov, and U. Feller, “Long-term field drought affects leaf protein pattern and chloroplast ultrastructure of winter wheat in a cultivar-specific manner,” J. Agron. Crop Sci. 198(2), 104–117 (2012).
[Crossref]

D. Díaz, D. W. Hahn, and A. Molina, “Evaluation of laser-induced breakdown spectroscopy (LIBS) as a measurement technique for evaluation of total elemental concentration in soils,” Appl. Spectrosc. 66(1), 99–106 (2012).
[Crossref]

D. Santos, L. C. Nunes, G. G. A. Carvalho, and F. J. Krug, “Laser-induced breakdown spectroscopy for analysis of plant materials: a review,” Spectrochim. Acta B At. Spectrosc. 71-72, 3–13 (2012).
[Crossref]

J. Kaiser, K. Novotny, M. Z. Martin, A. Hrdlicka, R. Malina, M. Hartl, V. Adam, and R. Kizek, “Trace elemental analysis by laser-induced breakdown spectroscopy – biological applications,” Surf. Sci. Rep. 67(11-12), 233–243 (2012).
[Crossref]

2011 (1)

D. Marcos-Martinez, J. A. Ayala, R. C. Izquierdo-Hornillos, F. J. de Villena, and J. O. Caceres, “Identification and discrimination of bacterial strains by laser induced breakdown spectroscopy and neural networks,” Talanta 84(3), 730–737 (2011).
[Crossref] [PubMed]

2010 (1)

D. Sun, S. Maugen, C. Dong, and X. Ma, “A semi-quantitative analysis of essential micronutrient in folium lycii using laser-induced breakdown spectroscopy technique,” Plasma Sci. Technol. 12(4), 478–481 (2010).
[Crossref]

2009 (1)

W. Lei, V. Motto-Ros, M. Boueri, Q. Ma, D. Zhang, L. Zheng, H. Zeng, and J. Yu, “Time-resolved characterization of laser-induced plasma from fresh potato,” Spectrochim. Acta B At. Spectrosc. 64(9), 891–898 (2009).
[Crossref]

2008 (3)

L. Eleuch, A. Jilal, S. Grando, S. Ceccarelli, M. Schmising, H. Tsujimoto, A. Hajer, A. Daaloul, and M. Baum, “Genetic diversity and association analysis for salinity tolerance, heading date and plant height of barley germplasm using simple sequence repeat markers,” J. Integr. Plant Biol. 50(8), 1004–1014 (2008).
[Crossref] [PubMed]

I. Slama, T. Ghnaya, A. Savouré, and C. Abdelly, “Combined effects of long-term salinity and soil drying on growth, water relations, nutrient status and proline accumulation of Sesuvium portulacastrum,” C. R. Biol. 331(6), 442–451 (2008).
[Crossref] [PubMed]

B. Bousquet, G. Travaillé, A. Ismaël, L. Canioni, K. Michel-Le Pierrès, E. Brasseur, S. Roy, I. le Hecho, M. Larregieu, S. Tellier, M. Potin-Gautier, T. Boriachon, P. Wazen, A. Diard, and S. Belbèze, “Development of a mobile system based on laser-induced breakdown spectroscopy and dedicated to in situ analysis of polluted soils,” Spectrochim. Acta B At. Spectrosc. 63(10), 1085–1090 (2008).
[Crossref]

2007 (2)

M. Galiova, J. Kaiser, K. Novotny, O. Samek, L. Raele, R. Malina, K. Palenikova, M. Liska, V. Cudek, V. Kanicky, V. Otruba, A. Poma, and A. Tucci, “Utilization of laser-induced breakdown spectroscopy for investigation of metal accumulation in vegetal tissue,” Spectrochim. Acta B At. Spectrosc. 62(12), 1597–1605 (2007).
[Crossref]

M. Bossu, H. Zuo-Qiang, M. Baudelet, Y. Jin, Z. Zhe, and Z. Jie, “Femtosecond laser-induced breakdown spectroscopy for detection of trace elements in Sophora leaves,” Chin. Phys. Lett. 24(12), 3466–3468 (2007).
[Crossref]

2006 (1)

O. Samek, J. Lambert, R. Hergenröder, M. Liška, J. Kaiser, K. Novotný, and S. Kukhlevsky, “Femtosecond laser spectrochemical analysis of plant samples,” Laser Phys. Lett. 3(1), 21–25 (2006).
[Crossref]

2004 (1)

G. Mejean, J. Kasparian, J. Yu, S. Frey, E. Salmon, and J. P. Wolf, “Remote detection and identification of biological aerosols using a femtosecond terawatt lidar system,” Appl. Phys. B 78, 535–537 (2004).
[Crossref]

2003 (3)

A. C. Samuels, F. C. DeLucia, K. L. McNesby, and A. W. Miziolek, “Laser-induced breakdown spectroscopy of bacterial spores, molds, pollens, and protein: initial studies of discrimination potential,” Appl. Opt. 42(30), 6205–6209 (2003).
[Crossref] [PubMed]

A. Assion, M. Wollenhaupt, L. Haag, F. Mayorov, C. Sharpe-Tudoran, M. Winter, U. Kutschera, and T. Baumert, “Femtosecond laser-induced-breakdown spectrometry for Ca2+ analysis of biological samples with high spatial resolution,” Appl. Phys. B 77(4), 391–397 (2003).
[Crossref]

J. P. Martìnez, J. F. Ledent, M. Bajji, J. M. Kinet, and S. Lutts, “Effect of water stress on growth, Na+ and K+ accumulation and water use efficiency,” J. Plant Growth Regul. 41(1), 63–73 (2003).
[Crossref]

2002 (1)

J. M. Pardo and F. J. Quintero, “Plants and sodium ions: keeping company with the enemy,” Genome Biol. 3(6), S1017 (2002).
[Crossref] [PubMed]

2000 (1)

H. K. Lichtenthaler and F. Babani, “Detection of photosynthetic activity and water stress by imaging the red chlorophyll fluorescence,” Plant Physiol. Biochem. 38(11), 889–895 (2000).
[Crossref]

1999 (2)

L. Chaerle, W. Van Caeneghem, E. Messens, H. Lambers, M. Van Montagu, and D. Van Der Straeten, “Presymptomatic visualization of plant-virus interactions by thermography,” Nat. Biotechnol. 17(8), 813–816 (1999).
[Crossref] [PubMed]

H. G. Jones, “Use of thermography for quantitative studies of spatial and temporal variation of stomatal conductance over leaf surfaces,” Plant Cell Environ. 22(9), 1043–1055 (1999).
[Crossref]

1998 (1)

J. Peñuelas and I. Filella, “Visible and nearinfrared reflectance techniques for diagnosing plant physiological status,” Trends Plant Sci. 3(4), 151–156 (1998).
[Crossref]

1997 (1)

H. Knight, A. J. Trewavas, and M. R. Knight, “Calcium signalling in Arabidopsis thaliana responding to drought and salinity,” Plant J. 12(5), 1067–1078 (1997).
[Crossref] [PubMed]

1996 (1)

H. K. Lichtenthaler, “Vegetation stress: an introduction to the stress concept in plants,” J. Plant Physiol. 148(1-2), 4–14 (1996).
[Crossref]

1995 (1)

R. B. Peterson and D. E. Aylor, “Chlorophyll fluorescence induction in leaves of Phaseolus vulgaris infected with bean rust (Uromycesappendiculatus),” Plant Physiol. 108(1), 163–171 (1995).
[Crossref] [PubMed]

1993 (1)

L. J. Wiles, H. J. Gold, and G. G. Wilkerson, “Modeling the uncertainty of weed density estimates to improve post-emergence herbicide control decisions,” Weed Res. 33(3), 241–252 (1993).
[Crossref]

1991 (1)

A. H. Price and G. A. F. Hendry, “Iron-catalysed oxygen radical formation and its possible contribution to drought damage in nine native grasses and three cereals,” Plant Cell Environ. 14(5), 477–484 (1991).
[Crossref]

1986 (1)

T. J. Flowers and A. R. Yeo, “Ion relations in plants under drought and salinity,” Aust. J. Plant Physiol. 13(1), 75 (1986).
[Crossref]

Abdelly, C.

I. Slama, T. Ghnaya, A. Savouré, and C. Abdelly, “Combined effects of long-term salinity and soil drying on growth, water relations, nutrient status and proline accumulation of Sesuvium portulacastrum,” C. R. Biol. 331(6), 442–451 (2008).
[Crossref] [PubMed]

Adam, V.

J. Kaiser, K. Novotny, M. Z. Martin, A. Hrdlicka, R. Malina, M. Hartl, V. Adam, and R. Kizek, “Trace elemental analysis by laser-induced breakdown spectroscopy – biological applications,” Surf. Sci. Rep. 67(11-12), 233–243 (2012).
[Crossref]

Adler, W.

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O. Samek, J. Lambert, R. Hergenröder, M. Liška, J. Kaiser, K. Novotný, and S. Kukhlevsky, “Femtosecond laser spectrochemical analysis of plant samples,” Laser Phys. Lett. 3(1), 21–25 (2006).
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O. Samek, J. Lambert, R. Hergenröder, M. Liška, J. Kaiser, K. Novotný, and S. Kukhlevsky, “Femtosecond laser spectrochemical analysis of plant samples,” Laser Phys. Lett. 3(1), 21–25 (2006).
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H. Chen, H. Li, Y. Sun, Y. Wang, and P. Lü, “Femtosecond laser for cavity preparation in enamel and dentin: ablation efficiency related factors,” Sci. Rep. 6(1), 20950 (2016).
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G. Mejean, J. Kasparian, J. Yu, S. Frey, E. Salmon, and J. P. Wolf, “Remote detection and identification of biological aerosols using a femtosecond terawatt lidar system,” Appl. Phys. B 78, 535–537 (2004).
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L. Chaerle, W. Van Caeneghem, E. Messens, H. Lambers, M. Van Montagu, and D. Van Der Straeten, “Presymptomatic visualization of plant-virus interactions by thermography,” Nat. Biotechnol. 17(8), 813–816 (1999).
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G. G. de Carvalho, J. Moros, D. Santos, F. J. Krug, and J. J. Laserna, “Direct determination of the nutrient profile in plant materials by femtosecond laser-induced breakdown spectroscopy,” Anal. Chim. Acta 876, 26–38 (2015).
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W. Lei, V. Motto-Ros, M. Boueri, Q. Ma, D. Zhang, L. Zheng, H. Zeng, and J. Yu, “Time-resolved characterization of laser-induced plasma from fresh potato,” Spectrochim. Acta B At. Spectrosc. 64(9), 891–898 (2009).
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K. Devey, M. Mucalo, G. Rajendram, and J. Lane, “Pasture vegetation elemental analysis by laser-induced breakdown spectroscopy,” Commun. Soil Sci. Plan. 46(S1), 72–80 (2015).
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J. Kaiser, K. Novotny, M. Z. Martin, A. Hrdlicka, R. Malina, M. Hartl, V. Adam, and R. Kizek, “Trace elemental analysis by laser-induced breakdown spectroscopy – biological applications,” Surf. Sci. Rep. 67(11-12), 233–243 (2012).
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M. Galiova, J. Kaiser, K. Novotny, O. Samek, L. Raele, R. Malina, K. Palenikova, M. Liska, V. Cudek, V. Kanicky, V. Otruba, A. Poma, and A. Tucci, “Utilization of laser-induced breakdown spectroscopy for investigation of metal accumulation in vegetal tissue,” Spectrochim. Acta B At. Spectrosc. 62(12), 1597–1605 (2007).
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O. Samek, J. Lambert, R. Hergenröder, M. Liška, J. Kaiser, K. Novotný, and S. Kukhlevsky, “Femtosecond laser spectrochemical analysis of plant samples,” Laser Phys. Lett. 3(1), 21–25 (2006).
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D. Santos, L. C. Nunes, G. G. A. Carvalho, and F. J. Krug, “Laser-induced breakdown spectroscopy for analysis of plant materials: a review,” Spectrochim. Acta B At. Spectrosc. 71-72, 3–13 (2012).
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M. Galiova, J. Kaiser, K. Novotny, O. Samek, L. Raele, R. Malina, K. Palenikova, M. Liska, V. Cudek, V. Kanicky, V. Otruba, A. Poma, and A. Tucci, “Utilization of laser-induced breakdown spectroscopy for investigation of metal accumulation in vegetal tissue,” Spectrochim. Acta B At. Spectrosc. 62(12), 1597–1605 (2007).
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M. Galiova, J. Kaiser, K. Novotny, O. Samek, L. Raele, R. Malina, K. Palenikova, M. Liska, V. Cudek, V. Kanicky, V. Otruba, A. Poma, and A. Tucci, “Utilization of laser-induced breakdown spectroscopy for investigation of metal accumulation in vegetal tissue,” Spectrochim. Acta B At. Spectrosc. 62(12), 1597–1605 (2007).
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K. Devey, M. Mucalo, G. Rajendram, and J. Lane, “Pasture vegetation elemental analysis by laser-induced breakdown spectroscopy,” Commun. Soil Sci. Plan. 46(S1), 72–80 (2015).
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R. Kanawade, F. Mahari, F. Klämpfl, M. Rohde, C. Knipfer, K. Tangermann-Gerk, W. Adler, M. Schmidt, and F. Stelzle, “Qualitative tissue differentiation by analysing the intensity ratios of atomic emission lines using laser induced breakdown spectroscopy (LIBS): prospects for a feedback mechanism for surgical laser systems,” J. Biophotonics 8(1-2), 153–161 (2015).
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Roy, S.

B. Bousquet, G. Travaillé, A. Ismaël, L. Canioni, K. Michel-Le Pierrès, E. Brasseur, S. Roy, I. le Hecho, M. Larregieu, S. Tellier, M. Potin-Gautier, T. Boriachon, P. Wazen, A. Diard, and S. Belbèze, “Development of a mobile system based on laser-induced breakdown spectroscopy and dedicated to in situ analysis of polluted soils,” Spectrochim. Acta B At. Spectrosc. 63(10), 1085–1090 (2008).
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J. J. Casanova, S. A. O’Shaughnessy, S. R. Evett, and C. M. Rush, “Development of a wireless computer vision instrument to detect biotic stress in wheat,” Sensors (Basel) 14(9), 17753–17769 (2014).
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G. Mejean, J. Kasparian, J. Yu, S. Frey, E. Salmon, and J. P. Wolf, “Remote detection and identification of biological aerosols using a femtosecond terawatt lidar system,” Appl. Phys. B 78, 535–537 (2004).
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M. Galiova, J. Kaiser, K. Novotny, O. Samek, L. Raele, R. Malina, K. Palenikova, M. Liska, V. Cudek, V. Kanicky, V. Otruba, A. Poma, and A. Tucci, “Utilization of laser-induced breakdown spectroscopy for investigation of metal accumulation in vegetal tissue,” Spectrochim. Acta B At. Spectrosc. 62(12), 1597–1605 (2007).
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Santos, D.

G. G. de Carvalho, J. Moros, D. Santos, F. J. Krug, and J. J. Laserna, “Direct determination of the nutrient profile in plant materials by femtosecond laser-induced breakdown spectroscopy,” Anal. Chim. Acta 876, 26–38 (2015).
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D. Santos, L. C. Nunes, G. G. A. Carvalho, and F. J. Krug, “Laser-induced breakdown spectroscopy for analysis of plant materials: a review,” Spectrochim. Acta B At. Spectrosc. 71-72, 3–13 (2012).
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A. A. Farjo, A. Sugar, S. C. Schallhorn, P. A. Majmudar, D. J. Tanzer, W. B. Trattler, J. B. Cason, K. E. Donaldson, and G. D. Kymionis, “Femtosecond lasers for LASIK flap creation: a report by the American Academy of Ophthalmology,” Ophthalmology 120(3), e5–e20 (2013).
[Crossref] [PubMed]

Schmidt, M.

R. Kanawade, F. Mahari, F. Klämpfl, M. Rohde, C. Knipfer, K. Tangermann-Gerk, W. Adler, M. Schmidt, and F. Stelzle, “Qualitative tissue differentiation by analysing the intensity ratios of atomic emission lines using laser induced breakdown spectroscopy (LIBS): prospects for a feedback mechanism for surgical laser systems,” J. Biophotonics 8(1-2), 153–161 (2015).
[Crossref] [PubMed]

Schmising, M.

L. Eleuch, A. Jilal, S. Grando, S. Ceccarelli, M. Schmising, H. Tsujimoto, A. Hajer, A. Daaloul, and M. Baum, “Genetic diversity and association analysis for salinity tolerance, heading date and plant height of barley germplasm using simple sequence repeat markers,” J. Integr. Plant Biol. 50(8), 1004–1014 (2008).
[Crossref] [PubMed]

Sharpe-Tudoran, C.

A. Assion, M. Wollenhaupt, L. Haag, F. Mayorov, C. Sharpe-Tudoran, M. Winter, U. Kutschera, and T. Baumert, “Femtosecond laser-induced-breakdown spectrometry for Ca2+ analysis of biological samples with high spatial resolution,” Appl. Phys. B 77(4), 391–397 (2003).
[Crossref]

Simova-Stoilova, L.

V. Vassileva, D. Demirevska, L. Simova-Stoilova, T. Petrova, N. Tsenov, and U. Feller, “Long-term field drought affects leaf protein pattern and chloroplast ultrastructure of winter wheat in a cultivar-specific manner,” J. Agron. Crop Sci. 198(2), 104–117 (2012).
[Crossref]

Slama, I.

I. Slama, T. Ghnaya, A. Savouré, and C. Abdelly, “Combined effects of long-term salinity and soil drying on growth, water relations, nutrient status and proline accumulation of Sesuvium portulacastrum,” C. R. Biol. 331(6), 442–451 (2008).
[Crossref] [PubMed]

Sorell, B. K.

K. Hancke, B. K. Sorell, L. C. Lund-Hansen, M. Larsen, T. Hancke, and R. N. Glud, “Effects of temperature and irradiance on a benthic microalgal community: a combined two-dimensional oxygen and fluorescence imaging approach,” Limnol. Oceanogr. 59(5), 1599–1611 (2014).
[Crossref]

Stelzle, F.

R. Kanawade, F. Mahari, F. Klämpfl, M. Rohde, C. Knipfer, K. Tangermann-Gerk, W. Adler, M. Schmidt, and F. Stelzle, “Qualitative tissue differentiation by analysing the intensity ratios of atomic emission lines using laser induced breakdown spectroscopy (LIBS): prospects for a feedback mechanism for surgical laser systems,” J. Biophotonics 8(1-2), 153–161 (2015).
[Crossref] [PubMed]

Sugar, A.

A. A. Farjo, A. Sugar, S. C. Schallhorn, P. A. Majmudar, D. J. Tanzer, W. B. Trattler, J. B. Cason, K. E. Donaldson, and G. D. Kymionis, “Femtosecond lasers for LASIK flap creation: a report by the American Academy of Ophthalmology,” Ophthalmology 120(3), e5–e20 (2013).
[Crossref] [PubMed]

Sun, D.

D. Sun, S. Maugen, C. Dong, and X. Ma, “A semi-quantitative analysis of essential micronutrient in folium lycii using laser-induced breakdown spectroscopy technique,” Plasma Sci. Technol. 12(4), 478–481 (2010).
[Crossref]

Sun, Y.

H. Chen, H. Li, Y. Sun, Y. Wang, and P. Lü, “Femtosecond laser for cavity preparation in enamel and dentin: ablation efficiency related factors,” Sci. Rep. 6(1), 20950 (2016).
[Crossref] [PubMed]

Tangermann-Gerk, K.

R. Kanawade, F. Mahari, F. Klämpfl, M. Rohde, C. Knipfer, K. Tangermann-Gerk, W. Adler, M. Schmidt, and F. Stelzle, “Qualitative tissue differentiation by analysing the intensity ratios of atomic emission lines using laser induced breakdown spectroscopy (LIBS): prospects for a feedback mechanism for surgical laser systems,” J. Biophotonics 8(1-2), 153–161 (2015).
[Crossref] [PubMed]

Tanzer, D. J.

A. A. Farjo, A. Sugar, S. C. Schallhorn, P. A. Majmudar, D. J. Tanzer, W. B. Trattler, J. B. Cason, K. E. Donaldson, and G. D. Kymionis, “Femtosecond lasers for LASIK flap creation: a report by the American Academy of Ophthalmology,” Ophthalmology 120(3), e5–e20 (2013).
[Crossref] [PubMed]

Tellier, S.

B. Bousquet, G. Travaillé, A. Ismaël, L. Canioni, K. Michel-Le Pierrès, E. Brasseur, S. Roy, I. le Hecho, M. Larregieu, S. Tellier, M. Potin-Gautier, T. Boriachon, P. Wazen, A. Diard, and S. Belbèze, “Development of a mobile system based on laser-induced breakdown spectroscopy and dedicated to in situ analysis of polluted soils,” Spectrochim. Acta B At. Spectrosc. 63(10), 1085–1090 (2008).
[Crossref]

Trattler, W. B.

A. A. Farjo, A. Sugar, S. C. Schallhorn, P. A. Majmudar, D. J. Tanzer, W. B. Trattler, J. B. Cason, K. E. Donaldson, and G. D. Kymionis, “Femtosecond lasers for LASIK flap creation: a report by the American Academy of Ophthalmology,” Ophthalmology 120(3), e5–e20 (2013).
[Crossref] [PubMed]

Travaillé, G.

B. Bousquet, G. Travaillé, A. Ismaël, L. Canioni, K. Michel-Le Pierrès, E. Brasseur, S. Roy, I. le Hecho, M. Larregieu, S. Tellier, M. Potin-Gautier, T. Boriachon, P. Wazen, A. Diard, and S. Belbèze, “Development of a mobile system based on laser-induced breakdown spectroscopy and dedicated to in situ analysis of polluted soils,” Spectrochim. Acta B At. Spectrosc. 63(10), 1085–1090 (2008).
[Crossref]

Trewavas, A. J.

H. Knight, A. J. Trewavas, and M. R. Knight, “Calcium signalling in Arabidopsis thaliana responding to drought and salinity,” Plant J. 12(5), 1067–1078 (1997).
[Crossref] [PubMed]

Tsenov, N.

V. Vassileva, D. Demirevska, L. Simova-Stoilova, T. Petrova, N. Tsenov, and U. Feller, “Long-term field drought affects leaf protein pattern and chloroplast ultrastructure of winter wheat in a cultivar-specific manner,” J. Agron. Crop Sci. 198(2), 104–117 (2012).
[Crossref]

Tsujimoto, H.

L. Eleuch, A. Jilal, S. Grando, S. Ceccarelli, M. Schmising, H. Tsujimoto, A. Hajer, A. Daaloul, and M. Baum, “Genetic diversity and association analysis for salinity tolerance, heading date and plant height of barley germplasm using simple sequence repeat markers,” J. Integr. Plant Biol. 50(8), 1004–1014 (2008).
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Tucci, A.

M. Galiova, J. Kaiser, K. Novotny, O. Samek, L. Raele, R. Malina, K. Palenikova, M. Liska, V. Cudek, V. Kanicky, V. Otruba, A. Poma, and A. Tucci, “Utilization of laser-induced breakdown spectroscopy for investigation of metal accumulation in vegetal tissue,” Spectrochim. Acta B At. Spectrosc. 62(12), 1597–1605 (2007).
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Tyystjärvi, E.

A. Porcar-Castell, E. Tyystjärvi, J. Atherton, C. van der Tol, J. Flexas, E. E. Pfündel, J. Moreno, C. Frankenberg, and J. A. Berry, “Linking chlorophyll a fluorescence to photosynthesis for remote sensing applications: mechanisms and challenges,” J. Exp. Bot. 65(15), 4065–4095 (2014).
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Van Caeneghem, W.

L. Chaerle, W. Van Caeneghem, E. Messens, H. Lambers, M. Van Montagu, and D. Van Der Straeten, “Presymptomatic visualization of plant-virus interactions by thermography,” Nat. Biotechnol. 17(8), 813–816 (1999).
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Van Der Straeten, D.

L. Chaerle, W. Van Caeneghem, E. Messens, H. Lambers, M. Van Montagu, and D. Van Der Straeten, “Presymptomatic visualization of plant-virus interactions by thermography,” Nat. Biotechnol. 17(8), 813–816 (1999).
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van der Tol, C.

A. Porcar-Castell, E. Tyystjärvi, J. Atherton, C. van der Tol, J. Flexas, E. E. Pfündel, J. Moreno, C. Frankenberg, and J. A. Berry, “Linking chlorophyll a fluorescence to photosynthesis for remote sensing applications: mechanisms and challenges,” J. Exp. Bot. 65(15), 4065–4095 (2014).
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Van Montagu, M.

L. Chaerle, W. Van Caeneghem, E. Messens, H. Lambers, M. Van Montagu, and D. Van Der Straeten, “Presymptomatic visualization of plant-virus interactions by thermography,” Nat. Biotechnol. 17(8), 813–816 (1999).
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Vassileva, V.

V. Vassileva, D. Demirevska, L. Simova-Stoilova, T. Petrova, N. Tsenov, and U. Feller, “Long-term field drought affects leaf protein pattern and chloroplast ultrastructure of winter wheat in a cultivar-specific manner,” J. Agron. Crop Sci. 198(2), 104–117 (2012).
[Crossref]

Vazquez de Aldana, J. R.

F. Chen and J. R. Vazquez de Aldana, “Optical waveguides in crystalline dielectric materials produced by femtosecond-laser micromachining,” Laser Photonics Rev. 8(2), 251–275 (2014).
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Wang, X.

S. Zhang, X. Wang, M. He, Y. Jiang, B. Zhang, W. Hang, and B. Huang, “Laser-induced plasma temperature,” Spectrochim. Acta B At. Spectrosc. 97, 13–33 (2014).
[Crossref]

Wang, Y.

H. Chen, H. Li, Y. Sun, Y. Wang, and P. Lü, “Femtosecond laser for cavity preparation in enamel and dentin: ablation efficiency related factors,” Sci. Rep. 6(1), 20950 (2016).
[Crossref] [PubMed]

Wazen, P.

B. Bousquet, G. Travaillé, A. Ismaël, L. Canioni, K. Michel-Le Pierrès, E. Brasseur, S. Roy, I. le Hecho, M. Larregieu, S. Tellier, M. Potin-Gautier, T. Boriachon, P. Wazen, A. Diard, and S. Belbèze, “Development of a mobile system based on laser-induced breakdown spectroscopy and dedicated to in situ analysis of polluted soils,” Spectrochim. Acta B At. Spectrosc. 63(10), 1085–1090 (2008).
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L. J. Wiles, H. J. Gold, and G. G. Wilkerson, “Modeling the uncertainty of weed density estimates to improve post-emergence herbicide control decisions,” Weed Res. 33(3), 241–252 (1993).
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A. Assion, M. Wollenhaupt, L. Haag, F. Mayorov, C. Sharpe-Tudoran, M. Winter, U. Kutschera, and T. Baumert, “Femtosecond laser-induced-breakdown spectrometry for Ca2+ analysis of biological samples with high spatial resolution,” Appl. Phys. B 77(4), 391–397 (2003).
[Crossref]

Wolf, J. P.

G. Mejean, J. Kasparian, J. Yu, S. Frey, E. Salmon, and J. P. Wolf, “Remote detection and identification of biological aerosols using a femtosecond terawatt lidar system,” Appl. Phys. B 78, 535–537 (2004).
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Wollenhaupt, M.

A. Assion, M. Wollenhaupt, L. Haag, F. Mayorov, C. Sharpe-Tudoran, M. Winter, U. Kutschera, and T. Baumert, “Femtosecond laser-induced-breakdown spectrometry for Ca2+ analysis of biological samples with high spatial resolution,” Appl. Phys. B 77(4), 391–397 (2003).
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I. M. Ahmed, F. Cao, M. Zhang, X. Chen, G. Zhang, and F. Wu, “Difference in yield and physiological features in response to drought and salinity combined stress during anthesis in Tibetan wild and cultivated barleys,” PLoS One 8(10), e77869 (2013).
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Wu, J.

Z. Dong, X. Zhou, J. Wu, Z. Zhang, T. Li, Z. Zhou, S. Zhang, and G. Li, “Small incision lenticule extraction (SMILE) and femtosecond laser LASIK: comparison of corneal wound healing and inflammation,” Br. J. Ophthalmol. 98(2), 263–269 (2014).
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Yeo, A. R.

T. J. Flowers and A. R. Yeo, “Ion relations in plants under drought and salinity,” Aust. J. Plant Physiol. 13(1), 75 (1986).
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Yu, J.

W. Lei, V. Motto-Ros, M. Boueri, Q. Ma, D. Zhang, L. Zheng, H. Zeng, and J. Yu, “Time-resolved characterization of laser-induced plasma from fresh potato,” Spectrochim. Acta B At. Spectrosc. 64(9), 891–898 (2009).
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G. Mejean, J. Kasparian, J. Yu, S. Frey, E. Salmon, and J. P. Wolf, “Remote detection and identification of biological aerosols using a femtosecond terawatt lidar system,” Appl. Phys. B 78, 535–537 (2004).
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Zeng, H.

W. Lei, V. Motto-Ros, M. Boueri, Q. Ma, D. Zhang, L. Zheng, H. Zeng, and J. Yu, “Time-resolved characterization of laser-induced plasma from fresh potato,” Spectrochim. Acta B At. Spectrosc. 64(9), 891–898 (2009).
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Zhang, B.

S. Zhang, X. Wang, M. He, Y. Jiang, B. Zhang, W. Hang, and B. Huang, “Laser-induced plasma temperature,” Spectrochim. Acta B At. Spectrosc. 97, 13–33 (2014).
[Crossref]

Zhang, D.

W. Lei, V. Motto-Ros, M. Boueri, Q. Ma, D. Zhang, L. Zheng, H. Zeng, and J. Yu, “Time-resolved characterization of laser-induced plasma from fresh potato,” Spectrochim. Acta B At. Spectrosc. 64(9), 891–898 (2009).
[Crossref]

Zhang, G.

I. M. Ahmed, F. Cao, M. Zhang, X. Chen, G. Zhang, and F. Wu, “Difference in yield and physiological features in response to drought and salinity combined stress during anthesis in Tibetan wild and cultivated barleys,” PLoS One 8(10), e77869 (2013).
[Crossref] [PubMed]

Zhang, M.

I. M. Ahmed, F. Cao, M. Zhang, X. Chen, G. Zhang, and F. Wu, “Difference in yield and physiological features in response to drought and salinity combined stress during anthesis in Tibetan wild and cultivated barleys,” PLoS One 8(10), e77869 (2013).
[Crossref] [PubMed]

Zhang, S.

S. Zhang, X. Wang, M. He, Y. Jiang, B. Zhang, W. Hang, and B. Huang, “Laser-induced plasma temperature,” Spectrochim. Acta B At. Spectrosc. 97, 13–33 (2014).
[Crossref]

Z. Dong, X. Zhou, J. Wu, Z. Zhang, T. Li, Z. Zhou, S. Zhang, and G. Li, “Small incision lenticule extraction (SMILE) and femtosecond laser LASIK: comparison of corneal wound healing and inflammation,” Br. J. Ophthalmol. 98(2), 263–269 (2014).
[PubMed]

Zhang, Z.

Z. Dong, X. Zhou, J. Wu, Z. Zhang, T. Li, Z. Zhou, S. Zhang, and G. Li, “Small incision lenticule extraction (SMILE) and femtosecond laser LASIK: comparison of corneal wound healing and inflammation,” Br. J. Ophthalmol. 98(2), 263–269 (2014).
[PubMed]

Zhe, Z.

M. Bossu, H. Zuo-Qiang, M. Baudelet, Y. Jin, Z. Zhe, and Z. Jie, “Femtosecond laser-induced breakdown spectroscopy for detection of trace elements in Sophora leaves,” Chin. Phys. Lett. 24(12), 3466–3468 (2007).
[Crossref]

Zheng, L.

W. Lei, V. Motto-Ros, M. Boueri, Q. Ma, D. Zhang, L. Zheng, H. Zeng, and J. Yu, “Time-resolved characterization of laser-induced plasma from fresh potato,” Spectrochim. Acta B At. Spectrosc. 64(9), 891–898 (2009).
[Crossref]

Zhou, X.

Z. Dong, X. Zhou, J. Wu, Z. Zhang, T. Li, Z. Zhou, S. Zhang, and G. Li, “Small incision lenticule extraction (SMILE) and femtosecond laser LASIK: comparison of corneal wound healing and inflammation,” Br. J. Ophthalmol. 98(2), 263–269 (2014).
[PubMed]

Zhou, Z.

Z. Dong, X. Zhou, J. Wu, Z. Zhang, T. Li, Z. Zhou, S. Zhang, and G. Li, “Small incision lenticule extraction (SMILE) and femtosecond laser LASIK: comparison of corneal wound healing and inflammation,” Br. J. Ophthalmol. 98(2), 263–269 (2014).
[PubMed]

Zuo-Qiang, H.

M. Bossu, H. Zuo-Qiang, M. Baudelet, Y. Jin, Z. Zhe, and Z. Jie, “Femtosecond laser-induced breakdown spectroscopy for detection of trace elements in Sophora leaves,” Chin. Phys. Lett. 24(12), 3466–3468 (2007).
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Anal. Chim. Acta (1)

G. G. de Carvalho, J. Moros, D. Santos, F. J. Krug, and J. J. Laserna, “Direct determination of the nutrient profile in plant materials by femtosecond laser-induced breakdown spectroscopy,” Anal. Chim. Acta 876, 26–38 (2015).
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Appl. Opt. (1)

Appl. Phys. B (2)

A. Assion, M. Wollenhaupt, L. Haag, F. Mayorov, C. Sharpe-Tudoran, M. Winter, U. Kutschera, and T. Baumert, “Femtosecond laser-induced-breakdown spectrometry for Ca2+ analysis of biological samples with high spatial resolution,” Appl. Phys. B 77(4), 391–397 (2003).
[Crossref]

G. Mejean, J. Kasparian, J. Yu, S. Frey, E. Salmon, and J. P. Wolf, “Remote detection and identification of biological aerosols using a femtosecond terawatt lidar system,” Appl. Phys. B 78, 535–537 (2004).
[Crossref]

Appl. Spectrosc. (1)

Aust. J. Plant Physiol. (1)

T. J. Flowers and A. R. Yeo, “Ion relations in plants under drought and salinity,” Aust. J. Plant Physiol. 13(1), 75 (1986).
[Crossref]

Br. J. Ophthalmol. (1)

Z. Dong, X. Zhou, J. Wu, Z. Zhang, T. Li, Z. Zhou, S. Zhang, and G. Li, “Small incision lenticule extraction (SMILE) and femtosecond laser LASIK: comparison of corneal wound healing and inflammation,” Br. J. Ophthalmol. 98(2), 263–269 (2014).
[PubMed]

C. R. Biol. (1)

I. Slama, T. Ghnaya, A. Savouré, and C. Abdelly, “Combined effects of long-term salinity and soil drying on growth, water relations, nutrient status and proline accumulation of Sesuvium portulacastrum,” C. R. Biol. 331(6), 442–451 (2008).
[Crossref] [PubMed]

Chin. Phys. Lett. (1)

M. Bossu, H. Zuo-Qiang, M. Baudelet, Y. Jin, Z. Zhe, and Z. Jie, “Femtosecond laser-induced breakdown spectroscopy for detection of trace elements in Sophora leaves,” Chin. Phys. Lett. 24(12), 3466–3468 (2007).
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Commun. Soil Sci. Plan. (1)

K. Devey, M. Mucalo, G. Rajendram, and J. Lane, “Pasture vegetation elemental analysis by laser-induced breakdown spectroscopy,” Commun. Soil Sci. Plan. 46(S1), 72–80 (2015).
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Genome Biol. (1)

J. M. Pardo and F. J. Quintero, “Plants and sodium ions: keeping company with the enemy,” Genome Biol. 3(6), S1017 (2002).
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J. Agron. Crop Sci. (1)

V. Vassileva, D. Demirevska, L. Simova-Stoilova, T. Petrova, N. Tsenov, and U. Feller, “Long-term field drought affects leaf protein pattern and chloroplast ultrastructure of winter wheat in a cultivar-specific manner,” J. Agron. Crop Sci. 198(2), 104–117 (2012).
[Crossref]

J. Biophotonics (1)

R. Kanawade, F. Mahari, F. Klämpfl, M. Rohde, C. Knipfer, K. Tangermann-Gerk, W. Adler, M. Schmidt, and F. Stelzle, “Qualitative tissue differentiation by analysing the intensity ratios of atomic emission lines using laser induced breakdown spectroscopy (LIBS): prospects for a feedback mechanism for surgical laser systems,” J. Biophotonics 8(1-2), 153–161 (2015).
[Crossref] [PubMed]

J. Exp. Bot. (1)

A. Porcar-Castell, E. Tyystjärvi, J. Atherton, C. van der Tol, J. Flexas, E. E. Pfündel, J. Moreno, C. Frankenberg, and J. A. Berry, “Linking chlorophyll a fluorescence to photosynthesis for remote sensing applications: mechanisms and challenges,” J. Exp. Bot. 65(15), 4065–4095 (2014).
[Crossref] [PubMed]

J. Integr. Plant Biol. (1)

L. Eleuch, A. Jilal, S. Grando, S. Ceccarelli, M. Schmising, H. Tsujimoto, A. Hajer, A. Daaloul, and M. Baum, “Genetic diversity and association analysis for salinity tolerance, heading date and plant height of barley germplasm using simple sequence repeat markers,” J. Integr. Plant Biol. 50(8), 1004–1014 (2008).
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J. Plant Growth Regul. (1)

J. P. Martìnez, J. F. Ledent, M. Bajji, J. M. Kinet, and S. Lutts, “Effect of water stress on growth, Na+ and K+ accumulation and water use efficiency,” J. Plant Growth Regul. 41(1), 63–73 (2003).
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Laser Photonics Rev. (1)

F. Chen and J. R. Vazquez de Aldana, “Optical waveguides in crystalline dielectric materials produced by femtosecond-laser micromachining,” Laser Photonics Rev. 8(2), 251–275 (2014).
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Laser Phys. Lett. (1)

O. Samek, J. Lambert, R. Hergenröder, M. Liška, J. Kaiser, K. Novotný, and S. Kukhlevsky, “Femtosecond laser spectrochemical analysis of plant samples,” Laser Phys. Lett. 3(1), 21–25 (2006).
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Limnol. Oceanogr. (1)

K. Hancke, B. K. Sorell, L. C. Lund-Hansen, M. Larsen, T. Hancke, and R. N. Glud, “Effects of temperature and irradiance on a benthic microalgal community: a combined two-dimensional oxygen and fluorescence imaging approach,” Limnol. Oceanogr. 59(5), 1599–1611 (2014).
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Nat. Biotechnol. (1)

L. Chaerle, W. Van Caeneghem, E. Messens, H. Lambers, M. Van Montagu, and D. Van Der Straeten, “Presymptomatic visualization of plant-virus interactions by thermography,” Nat. Biotechnol. 17(8), 813–816 (1999).
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Ophthalmology (1)

A. A. Farjo, A. Sugar, S. C. Schallhorn, P. A. Majmudar, D. J. Tanzer, W. B. Trattler, J. B. Cason, K. E. Donaldson, and G. D. Kymionis, “Femtosecond lasers for LASIK flap creation: a report by the American Academy of Ophthalmology,” Ophthalmology 120(3), e5–e20 (2013).
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Plant Cell Environ. (2)

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H. Knight, A. J. Trewavas, and M. R. Knight, “Calcium signalling in Arabidopsis thaliana responding to drought and salinity,” Plant J. 12(5), 1067–1078 (1997).
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Plant Physiol. (1)

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Plasma Sci. Technol. (1)

D. Sun, S. Maugen, C. Dong, and X. Ma, “A semi-quantitative analysis of essential micronutrient in folium lycii using laser-induced breakdown spectroscopy technique,” Plasma Sci. Technol. 12(4), 478–481 (2010).
[Crossref]

PLoS One (1)

I. M. Ahmed, F. Cao, M. Zhang, X. Chen, G. Zhang, and F. Wu, “Difference in yield and physiological features in response to drought and salinity combined stress during anthesis in Tibetan wild and cultivated barleys,” PLoS One 8(10), e77869 (2013).
[Crossref] [PubMed]

Sci. Rep. (1)

H. Chen, H. Li, Y. Sun, Y. Wang, and P. Lü, “Femtosecond laser for cavity preparation in enamel and dentin: ablation efficiency related factors,” Sci. Rep. 6(1), 20950 (2016).
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Sensors (Basel) (1)

J. J. Casanova, S. A. O’Shaughnessy, S. R. Evett, and C. M. Rush, “Development of a wireless computer vision instrument to detect biotic stress in wheat,” Sensors (Basel) 14(9), 17753–17769 (2014).
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Spectrochim. Acta B At. Spectrosc. (6)

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Figures (5)

Fig. 1
Fig. 1 Visual signatures of drought stress and water content. Photographs of gardenia (a) and wheat (c) plants on the first and last days of the treatment periods for both watered and non-watered treatment groups. Corresponding plots showing relative water content (% of day 0) for gardenia (b) and wheat (d) plants for the entire treatment periods.
Fig. 2
Fig. 2 Atomic spectral signatures of abiotic stress in gardenia and wheat. Schematic of the LIBS experiment on a non-stressed (a) and stressed (b) plant. A high intensity beam of femtosecond laser pulses is focused onto the surface of a plant leaf generating emission of light from atomic components of laser-induced hot plasma. LIBS spectra of gardenia (c) – (g) and wheat (h) – (l) plants: (c) and (h) show LIBS signals collected in the selected full spectral range on the first (black line) and last (red line) days of the treatment for the stressed plants; spectral regions of interest show relative changes in the LIBS signals of watered (d, e, i, j) and non-watered (f, g, k, l) plants on the first (black line) and last (red line) days of treatment. Peak assignments of major LIBS signals are shown in (c) and (h). Na, K and Fe peaks which are used for detection of plant stress are highlighted. The shown spectra are averages of twenty LIBS spectra from each sample.
Fig. 3
Fig. 3 Temporal evolution of nutrient LIBS signals and plasma temperature. (a) Difference in average peak intensities (rms) between watered and non-watered plants for the selected Na, Ca and Fe elements observed in the LIBS spectra of gardenia (yellow bars) and wheat (green bars) plants. (b) Difference in average plasma temperatures (rms) between watered and non-watered plants. Temporal evolution of nutrient LIBS signals and plasma temperatures for the watered (blue circles) and non-watered (orange circles) gardenia (i) – (iv) and wheat (I) – (IV) plants during the entire treatment periods. Dashed lines show quadratic curves-of-growth of specified peaks for the non-watered samples.
Fig. 4
Fig. 4 Temporal evolution of relative nutrient contents. (a) Difference in peak ratios (rms) between watered and non-watered plants for the selected Na, Ca and Fe elements observed in the LIBS spectra of gardenia (yellow bars) and wheat (green bars) plants. Temporal evolution of relative nutrient contents for the watered (blue circles) and non-watered (orange circles) gardenia (i) – (iv) and wheat (I) – (IV) plants during the entire treatment periods.
Fig. 5
Fig. 5 Schematic of the laser-induced breakdown spectroscopy (LIBS) performed on a leaf sample (inset).

Tables (1)

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Table 1 Peak assignments of the observed LIBS signals based on the NIST atomic spectral database [34].

Equations (2)

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I= hνAN 4π =( hc N 0 gA 4πλZ ) e ( E k b T ) , 
ln( Iλ gA )= E k b T ln( 4πZ hc N 0 ), 

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