from oxidative challenge. Biochim Biophys
Acta Bioenerg 1787:468–475
41. Bratt A, Rosenwasser S, Meyer A, Fluhr R
(2016) Organelle redox autonomy during
environmental stress. Plant Cell Environ
39:1909–1919
42. Baird GS, Zacharias DA, Tsien RY (1999) Circular permutation and receptor insertion
within green fluorescent proteins. Proc Natl
Acad Sci U S A 96:11241–11246
43. Nakai J, Ohkura M, Imoto K (2001) A high
signal-to-noise Ca
2+ probe composed of a single green fluorescent protein. Nat Biotechnol
19:137–141
44. Defalco TA, Toyota M, Phan V, Karia P,
Moeder W, Gilroy S, Yoshioka K (2017)
Using GCaMP3 to study Ca
2+ signaling in
Nicotiana species. Plant Cell Physiol
58:1173–1184
45. Kleist TJ, Cartwright HN, Perera AM, Christianson ML, Lemaux PG, Luan S (2017)
Genetically encoded calcium indicators for
fluorescence imaging in the moss Physcomitrella: GCaMP3 provides a bright new look.
Plant Biotechnol J 15:1235–1237
46. Vincent TR, Canham J, Toyota M,
Avramova M, Mugford ST, Gilroy S et al
(2017) Real-time in vivo recording of Arabidopsis calcium signals during insect feeding
using a fluorescent biosensor. J Vis Exp
(126):56142
47. Toyota M, Spencer D, Sawai-Toyota S, Jiaqi W,
Zhang T, Koo AJ et al (2018) Glutamate triggers long-distance, calcium-based plant
defense signaling. Science 361:1112–1115
48. Nguyen CT, Kurenda A, Stolz S, Che ´telat A,
Farmer EE (2018) Identification of cell populations necessary for leaf-to-leaf electrical signaling in a wounded plant. Proc Natl Acad Sci
U S A 115:10178–10183
49. Kalko EKV, Dukas R, Ratcliffe JM, Teeling EC,
Haven N, Fattu JM et al (2011) An expanded
palette of genetically. Science 557:1888–1891
50. Keinath NF, Waadt R, Brugman R, Schroeder
JI, Grossmann G, Schumacher K, Krebs M
(2015) Live cell imaging with R-GECO1
sheds light on flg22- and chitin-induced transient [Ca
2+
]cyt patterns in Arabidopsis. Mol
Plant 8:1188–1200
51. Belousov VV, Fradkov AF, Lukyanov KA, Staroverov DB, Shakhbazov KS, Terskikh AV,
Lukyanov S (2006) Genetically encoded fluorescent indicator for intracellular hydrogen
peroxide. Nat Methods 3:281–286
52. Markvicheva KN, Bilan DS, Mishina NM, Gorokhovatsky AY, Vinokurov LM, Lukyanov S,
Belousov VV (2011) A genetically encoded
sensor for H 2 O 2 with expanded dynamic
range. Bioorg Med Chem 19:1079–1084
53. Costa A, Drago I, Behera S, Zottini M, Pizzo P,
Schroeder JI et al (2010) H 2 O 2 in plant peroxisomes: an in vivo analysis uncovers a Ca
2+
-
dependent scavenging system. Plant J
62:760–772
54. Herna ´ndez-Barrera A, Velarde-Buendı ´a A,
Zepeda I, Sanchez F, Quinto C, Sa ´nchezLopez R et al (2015) Hyper, a hydrogen peroxide sensor, indicates the sensitivity of the
Arabidopsis root elongation zone to aluminum
treatment. Sensors 15:855–867
55. Exposito-Rodriguez M, Laissue PP, YvonDurocher G, Smirnoff N, Mullineaux PM
(2017)
Photosynthesis-dependent
H 2 O 2
transfer from chloroplasts to nuclei provides a
high-light signalling mechanism. Nat Commun 8:1–10
56. Marvin JS, Borghuis BG, Tian L, Cichon J,
Harnett MT, Akerboom J et al (2013) An optimized fluorescent probe for visualizing glutamate neurotransmission. Nat Methods
10:162–170
57. Mousavi SAR, Chauvin A, Pascaud F,
Kellenberger S, Farmer EE (2013) Glutamate
receptor-like genes mediate leaf-to-leaf wound
signalling. Nature 500:422–426
58. Pe ´rez Koldenkova V, Nagai T (2013) Genetically encoded Ca
2+ indicators: properties and
evaluation.
Biochim
Biophys
Acta
1833:1787–1797
59. Waadt R, Krebs M, Kudla J, Schumacher K
(2017) Multiparameter imaging of calcium
and abscisic acid and high-resolution quantitative calcium measurements using R-GECO1mTurquoise in Arabidopsis. New Phytol
216:303–320
60. Ast C, Foret J, Oltrogge LM, De Michele R,
Kleist TJ, Ho C-H, Frommer WB (2017)
Ratiometric Matryoshka biosensors from a
nested cassette of green- and orange-emitting
fluorescent proteins. Nat Commun 8:431
61. De Michele R, Ast C, Loque ´ D, Ho C-H, LA
Andrade S, Lanquar V et al (2013) Fluorescent
sensors reporting the activity of ammonium
transceptors in live cells. elife 2:1–22
62. Chaudhuri B, Ho ¨rmann F, Frommer WB
(2011) Dynamic imaging of glucose flux
impedance using FRET sensors in wild-type
Arabidopsis plants. J Exp Bot 62:2411–2417
63. Ho C-H, Frommer WB (2014) Fluorescent
sensors for activity and regulation of the nitrate
transceptor CHL1/NRT1.1 and oligopeptide
transporters. elife 3:1–21
64. Benfey PN, Chua N-H (1990) The cauliflower
mosaic virus 35S promoter: combinatorial
The Use of Genetically Encoded Fluorescent Biosensors
321
Acta Bioenerg 1787:468–475
41. Bratt A, Rosenwasser S, Meyer A, Fluhr R
(2016) Organelle redox autonomy during
environmental stress. Plant Cell Environ
39:1909–1919
42. Baird GS, Zacharias DA, Tsien RY (1999) Circular permutation and receptor insertion
within green fluorescent proteins. Proc Natl
Acad Sci U S A 96:11241–11246
43. Nakai J, Ohkura M, Imoto K (2001) A high
signal-to-noise Ca
2+ probe composed of a single green fluorescent protein. Nat Biotechnol
19:137–141
44. Defalco TA, Toyota M, Phan V, Karia P,
Moeder W, Gilroy S, Yoshioka K (2017)
Using GCaMP3 to study Ca
2+ signaling in
Nicotiana species. Plant Cell Physiol
58:1173–1184
45. Kleist TJ, Cartwright HN, Perera AM, Christianson ML, Lemaux PG, Luan S (2017)
Genetically encoded calcium indicators for
fluorescence imaging in the moss Physcomitrella: GCaMP3 provides a bright new look.
Plant Biotechnol J 15:1235–1237
46. Vincent TR, Canham J, Toyota M,
Avramova M, Mugford ST, Gilroy S et al
(2017) Real-time in vivo recording of Arabidopsis calcium signals during insect feeding
using a fluorescent biosensor. J Vis Exp
(126):56142
47. Toyota M, Spencer D, Sawai-Toyota S, Jiaqi W,
Zhang T, Koo AJ et al (2018) Glutamate triggers long-distance, calcium-based plant
defense signaling. Science 361:1112–1115
48. Nguyen CT, Kurenda A, Stolz S, Che ´telat A,
Farmer EE (2018) Identification of cell populations necessary for leaf-to-leaf electrical signaling in a wounded plant. Proc Natl Acad Sci
U S A 115:10178–10183
49. Kalko EKV, Dukas R, Ratcliffe JM, Teeling EC,
Haven N, Fattu JM et al (2011) An expanded
palette of genetically. Science 557:1888–1891
50. Keinath NF, Waadt R, Brugman R, Schroeder
JI, Grossmann G, Schumacher K, Krebs M
(2015) Live cell imaging with R-GECO1
sheds light on flg22- and chitin-induced transient [Ca
2+
]cyt patterns in Arabidopsis. Mol
Plant 8:1188–1200
51. Belousov VV, Fradkov AF, Lukyanov KA, Staroverov DB, Shakhbazov KS, Terskikh AV,
Lukyanov S (2006) Genetically encoded fluorescent indicator for intracellular hydrogen
peroxide. Nat Methods 3:281–286
52. Markvicheva KN, Bilan DS, Mishina NM, Gorokhovatsky AY, Vinokurov LM, Lukyanov S,
Belousov VV (2011) A genetically encoded
sensor for H 2 O 2 with expanded dynamic
range. Bioorg Med Chem 19:1079–1084
53. Costa A, Drago I, Behera S, Zottini M, Pizzo P,
Schroeder JI et al (2010) H 2 O 2 in plant peroxisomes: an in vivo analysis uncovers a Ca
2+
-
dependent scavenging system. Plant J
62:760–772
54. Herna ´ndez-Barrera A, Velarde-Buendı ´a A,
Zepeda I, Sanchez F, Quinto C, Sa ´nchezLopez R et al (2015) Hyper, a hydrogen peroxide sensor, indicates the sensitivity of the
Arabidopsis root elongation zone to aluminum
treatment. Sensors 15:855–867
55. Exposito-Rodriguez M, Laissue PP, YvonDurocher G, Smirnoff N, Mullineaux PM
(2017)
Photosynthesis-dependent
H 2 O 2
transfer from chloroplasts to nuclei provides a
high-light signalling mechanism. Nat Commun 8:1–10
56. Marvin JS, Borghuis BG, Tian L, Cichon J,
Harnett MT, Akerboom J et al (2013) An optimized fluorescent probe for visualizing glutamate neurotransmission. Nat Methods
10:162–170
57. Mousavi SAR, Chauvin A, Pascaud F,
Kellenberger S, Farmer EE (2013) Glutamate
receptor-like genes mediate leaf-to-leaf wound
signalling. Nature 500:422–426
58. Pe ´rez Koldenkova V, Nagai T (2013) Genetically encoded Ca
2+ indicators: properties and
evaluation.
Biochim
Biophys
Acta
1833:1787–1797
59. Waadt R, Krebs M, Kudla J, Schumacher K
(2017) Multiparameter imaging of calcium
and abscisic acid and high-resolution quantitative calcium measurements using R-GECO1mTurquoise in Arabidopsis. New Phytol
216:303–320
60. Ast C, Foret J, Oltrogge LM, De Michele R,
Kleist TJ, Ho C-H, Frommer WB (2017)
Ratiometric Matryoshka biosensors from a
nested cassette of green- and orange-emitting
fluorescent proteins. Nat Commun 8:431
61. De Michele R, Ast C, Loque ´ D, Ho C-H, LA
Andrade S, Lanquar V et al (2013) Fluorescent
sensors reporting the activity of ammonium
transceptors in live cells. elife 2:1–22
62. Chaudhuri B, Ho ¨rmann F, Frommer WB
(2011) Dynamic imaging of glucose flux
impedance using FRET sensors in wild-type
Arabidopsis plants. J Exp Bot 62:2411–2417
63. Ho C-H, Frommer WB (2014) Fluorescent
sensors for activity and regulation of the nitrate
transceptor CHL1/NRT1.1 and oligopeptide
transporters. elife 3:1–21
64. Benfey PN, Chua N-H (1990) The cauliflower
mosaic virus 35S promoter: combinatorial
The Use of Genetically Encoded Fluorescent Biosensors
321