Phytochrome B integrates light and temperature signals in Arabidopsis

TLDR: It is demonstrated that the phytochrome B (phyB) photoreceptor participates in temperature perception through its temperature-dependent reversion from the active Pfr state to the inactive Pr state, and proposed that in addition to its photorecept functions, phyB is a temperature sensor in plants.

Abstract: Ambient temperature regulates many aspects of plant growth and development, but its sensors are unknown. Here, we demonstrate that the phytochrome B (phyB) photoreceptor participates in temperature perception through its temperature-dependent reversion from the active Pfr state to the inactive Pr state. Increased rates of thermal reversion upon exposing Arabidopsis seedlings to warm environments reduce both the abundance of the biologically active Pfr-Pfr dimer pool of phyB and the size of the associated nuclear bodies, even in daylight. Mathematical analysis of stem growth for seedlings expressing wild-type phyB or thermally stable variants under various combinations of light and temperature revealed that phyB is physiologically responsive to both signals. We therefore propose that in addition to its photoreceptor functions, phyB is a temperature sensor in plants.

Full text

Washington University in St. Louis
Washington University Open Scholarship
0636.?(*;3:?!;)30*(:0659!8,9,5:(:0659 0636.?

Phytochrome B integrates light and temperature
signals in Arabidopsis
Martina Legris
Cornelia Klose
E Sethe Burgie
Cecilia Costigliolo Rojas Rojas
Maximiliano Neme
See next page for additional authors
6336=:/09(5+(++0:065(3=6829(:
/C7967,59*/63(89/07=;9:3,+;)06'-(*7;)9
!(8:6-:/, 06*/,409:8?644659 0636.?644659(5+:/, !3(5:0636.?644659
B098:0*3,09)86;./::6?6;-68-8,,(5+67,5(**,99)?:/,0636.?(:&(9/05.:65$50<,890:? 7,5#*/63(89/07:/(9),,5(**,7:,+-6805*3;906505
0636.?(*;3:?!;)30*(:0659!8,9,5:(:0659)?(5(;:/680@,+(+40509:8(:686-&(9/05.:65$50<,890:? 7,5#*/63(89/0768468,05-684(:065
73,(9,*65:(*:
+0.0:(3=;4(03=;9:3,+;
",*644,5+,+0:(:065
,.809(8:05(369,685,30(;8.0,#,:/,"61(9"61(9,*030(69:0.30636,4,(>04030(5603:)8;55,85+8,(9&0..,
!/0307#*/A-,8),8/(8+%0,89:8("0*/(8+(5+(9(368.,!/?:6*/864,05:,.8(:,930./:(5+:,47,8(:;8,90.5(3905
8()0+67909 Biology Faculty Publications & Presentations
/C7967,59*/63(89/07=;9:3,+;)06'-(*7;)9

Authors
(8:05(,.809685,30(369,#,:/,;8.0,,*030(69:0.30636"61(9"61(9(>04030(56,4,5+8,(9
03:)8;55,8!/0307&0..,),8/(8+#*/A-,8"0*/(8+%0,89:8((5+68.,(9(3
B09(8:0*3,09(<(03()3,(:&(9/05.:65$50<,890:? 7,5#*/63(89/07 /C7967,59*/63(89/07=;9:3,+;)06'-(*7;)9

Submitted Manuscript: Confidential
Title:
Phytochrome B integrates light and temperature signals in Arabidopsis
Authors: Martina Legris
1
, Cornelia Klose
2,†
, E. Sethe Burgie
3,†
,
Cecilia Costigliolo
1,†
,
Maximiliano Neme
1
, Andreas Hiltbrunner
2,4
, Philip A. Wigge
5
, Eberhard Schäfer
2,4,‡
,
Richard D. Vierstra
3,‡
, Jorge J. Casal
1,6,*
Affiliations:
1
Fundación Instituto Leloir, Instituto de Investigaciones Bioquímicas de Buenos Aires–
CONICET, 1405 Buenos Aires, Argentina
2
Institut für Biologie II, University of Freiburg, Schaenzlestr. 1, D-79104 Freiburg.
3
Department of Biology, Washington University in St. Louis, Campus Box 1137, One Brookings
Drive, St. Louis, MO 63130, USA
4
BIOSS Centre for Biological Signaling Studies, University of Freiburg, Schaenzlestr. 18, 79104
Freiburg, Germany
5
Sainsbury Laboratory, Cambridge University, 47 Bateman St. Cambridge CB2 1LR, UK
6
IFEVA, Facultad de Agronomía, Universidad de Buenos Aires and CONICET, Av. San Martín
4453, 1417 Buenos Aires, Argentina.
*Correspondence to: casal@ifeva.edu.ar.
†
These authors contributed equally.
‡
These authors contributed equally.

Legris et al. 2
Abstract:
Ambient temperature regulates many aspects of plant growth and development but its sensors are
unknown. Here, we demonstrate that the phytochrome B (phyB) photoreceptor participates in
temperature perception through its temperature-dependent reversion from the active Pfr state to
the inactive Pr state. Increased rates of thermal reversion upon exposing Arabidopsis seedlings to
warm environments reduce both the abundance of the biologically active Pfr-Pfr dimer pool of
phyB and the size of the associated nuclear bodies, even in daylight. Mathematical analysis of
stem growth for seedlings expressing wild-type phyB or thermally stable variants under various
combinations of light and temperature revealed that phyB is physiologically responsive to both
signals. We therefore propose that in addition to its photoreceptor functions, phyB is a
temperature sensor in plants.
One Sentence Summary:
Activity of the red-light photoreceptor phytochrome B is modulated by temperature.

Legris et al. 3
Main Text:
Plants have the capacity to adjust their growth and development in response to light and
temperature cues (1). Temperature sensing helps plants determine when to germinate, adjust their
body plan to protect themselves from adverse temperatures, and flower. Warm temperatures as
well as reduced light resulting from vegetative shade promote stem growth, enabling seedlings to
avoid heat stress and canopy shade from neighboring plants. Whereas light perception is driven
by a collection of identified photoreceptors, including the red/far-red light-absorbing
phytochromes, the blue/UV-A light-absorbing cryptochromes, phototropins, and members of the
Zeitlupe family, and the UV-B-absorbing UVR8 (2), temperature sensors remain to be
established (3). Finding the identit(ies) of temperature sensors would be of particular relevance
in the context of climate change (4).
Phytochrome B (phyB) is the main photoreceptor controlling growth in Arabidopsis
seedlings exposed to different shade conditions (5). Like others in the phytochrome family, phyB
is a homodimeric chromoprotein with each subunit harboring a covalently bound
phytochromobilin chromophore. phyB exists in two photo-interconvertible forms, a red-light
absorbing Pr state that is biologically inactive and a far-red light-absorbing Pfr state that is
biologically active (6, 7). Whereas Pr arises upon assembly with the bilin, formation of Pfr
requires light and its levels are strongly influenced by the red/far-red light ratio. Consequently,
because red light is absorbed by photosynthetic pigments, shade light from neighboring
vegetation has a strong impact on Pfr levels by reducing this ratio (8). phyB Pfr also
spontaneously reverts back to Pr in a light-independent reaction called thermal reversion (9–11).
Traditionally, thermal reversion was assumed to be too slow relative to the light reactions to