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PMID: 34155145 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Warm nights disrupt transcriptome rhythms in field-grown rice panicles.

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 118 ·No. 25 ·2021-00-22

Desai JS, Lawas LMF, Valente AM, Leman AR, Grinevich DO, Jagadish SVK, Doherty CJ

Abstract

In rice, a small increase in nighttime temperature reduces grain yield and quality. How warm nighttime temperatures (WNT) produce these detrimental effects is not well understood, especially in field conditions where the typical day-to-night temperature fluctuation exceeds the mild increase in nighttime temperature. We observed genome-wide disruption of gene expression timing during the reproductive phase in field-grown rice panicles acclimated to 2 to 3 °C WNT. Transcripts previously identified as rhythmically expressed with a 24-h period and circadian-regulated transcripts were more sensitive to WNT than were nonrhythmic transcripts. The system-wide perturbations in transcript levels suggest that WNT disrupt the tight temporal coordination between internal molecular events and the environment, resulting in reduced productivity. We identified transcriptional regulators whose predicted targets are enriched for sensitivity to WNT. The affected transcripts and candidate regulators identified through our network analysis explain molecular mechanisms driving sensitivity to WNT and identify candidates that can be targeted to enhance tolerance to WNT.

Keywords
circadian regulators climate change impact diel transcriptional networks global food security nighttime temperature increase
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Desai Jigar S ORCID
Department of Molecular and Structural Biochemistry, North Carolina State University, Raleigh, NC 27695.
Lawas Lovely Mae F
International Rice Research Institute, 1226 Metro Manila, Philippines.
Valente Ashlee M ORCID
Mimetics LLC, Durham, NC 27709.
Leman Adam R ORCID
Mimetics LLC, Durham, NC 27709.
Grinevich Dmitry O
Department of Molecular and Structural Biochemistry, North Carolina State University, Raleigh, NC 27695.
Jagadish S V Krishna ORCID
International Rice Research Institute, 1226 Metro Manila, Philippines; kjagadish@ksu.edu colleen_doherty@ncsu.edu. | Department of Agronomy, Kansas State University, Manhattan, KS 66506.
Doherty Colleen J ORCID
Department of Molecular and Structural Biochemistry, North Carolina State University, Raleigh, NC 27695; kjagadish@ksu.edu colleen_doherty@ncsu.edu.
Conflict of Interest

Competing interest statement: A.R.L. and A.M.V. are employed by Mimetics LLC.

References (81)
81 references, click to expand
  1. Damage to photosystem II due to heat stress without light-driven electron flow: involvement of enhanced introduction of reducing power into thylakoid membranes.
    Planta. 2012 Aug;236(2):753-61 PMID: 22526503
  2. RiceFREND: a platform for retrieving coexpressed gene networks in rice.
    Nucleic Acids Res. 2013 Jan;41(Database issue):D1214-21 PMID: 23180784
  3. Light and the circadian clock mediate time-specific changes in sensitivity to UV-B stress under light/dark cycles.
    J Exp Bot. 2014 Nov;65(20):6003-12 PMID: 25147271
  4. The Local Edge Machine: inference of dynamic models of gene regulation.
    Genome Biol. 2016 Oct 19;17(1):214 PMID: 27760556
  5. Daytime temperature is sensed by phytochrome B in Arabidopsis through a transcriptional activator HEMERA.
    Nat Commun. 2019 Jan 11;10(1):140 PMID: 30635559
  6. Global variation in diurnal asymmetry in temperature, cloud cover, specific humidity and precipitation and its association with leaf area index.
    Glob Chang Biol. 2020 Dec;26(12):7099-7111 PMID: 32998181
  7. The LNK1 night light-inducible and clock-regulated gene is induced also in response to warm-night through the circadian clock nighttime repressor in Arabidopsis thaliana.
    Plant Signal Behav. 2014;9(3):e28505 PMID: 24690904
  8. Circadian control of carbohydrate availability for growth in Arabidopsis plants at night.
    Proc Natl Acad Sci U S A. 2010 May 18;107(20):9458-63 PMID: 20439704
  9. Carbohydrate Level and Growth of Tomato Plants: II. The Effect of Irradiance and Temperature.
    Plant Physiol. 1986 Aug;81(4):1075-9 PMID: 16664946
  10. Heat shock-induced fluctuations in clock and light signaling enhance phytochrome B-mediated Arabidopsis deetiolation.
    Plant Cell. 2013 Aug;25(8):2892-906 PMID: 23933882
  11. Network discovery pipeline elucidates conserved time-of-day-specific cis-regulatory modules.
    PLoS Genet. 2008 Feb;4(2):e14 PMID: 18248097
  12. Circadian topology of metabolism.
    Nature. 2012 Nov 15;491(7424):348-56 PMID: 23151577
  13. PCH1 integrates circadian and light-signaling pathways to control photoperiod-responsive growth in Arabidopsis.
    Elife. 2016 Feb 03;5:e13292 PMID: 26839287
  14. Acclimation of foliar respiration and photosynthesis in response to experimental warming in a temperate steppe in northern China.
    PLoS One. 2013;8(2):e56482 PMID: 23457574
  15. ELF3 encodes a circadian clock-regulated nuclear protein that functions in an Arabidopsis PHYB signal transduction pathway.
    Plant Cell. 2001 Jun;13(6):1293-304 PMID: 11402161
  16. PSEUDO-RESPONSE REGULATOR 7 and 9 are partially redundant genes essential for the temperature responsiveness of the Arabidopsis circadian clock.
    Plant Cell. 2005 Mar;17(3):791-803 PMID: 15705949
  17. The regulation of UV-B responses by the circadian clock.
    Plant Signal Behav. 2015;10(5):e1000164 PMID: 26039469
  18. High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis.
    Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):7197-202 PMID: 9618562
  19. Rice yields decline with higher night temperature from global warming.
    Proc Natl Acad Sci U S A. 2004 Jul 6;101(27):9971-5 PMID: 15226500
  20. Plants under continuous light.
    Trends Plant Sci. 2011 Jun;16(6):310-8 PMID: 21396878
  21. Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock.
    Plant Physiol. 2005 Mar;137(3):961-8 PMID: 15728337
  22. Starch and the clock: the dark side of plant productivity.
    Trends Plant Sci. 2011 Mar;16(3):169-75 PMID: 21216654
  23. The evening complex coordinates environmental and endogenous signals in Arabidopsis.
    Nat Plants. 2017 Jun 26;3:17087 PMID: 28650433
  24. Punctual transcriptional regulation by the rice circadian clock under fluctuating field conditions.
    Plant Cell. 2015 Mar;27(3):633-48 PMID: 25757473
  25. Expanding Roles of PIFs in Signal Integration from Multiple Processes.
    Mol Plant. 2017 Aug 7;10(8):1035-1046 PMID: 28711729
  26. Temperature increase reduces global yields of major crops in four independent estimates.
    Proc Natl Acad Sci U S A. 2017 Aug 29;114(35):9326-9331 PMID: 28811375
  27. Novel transcriptional responses to heat revealed by turning up the heat at night.
    Plant Mol Biol. 2019 Sep;101(1-2):1-19 PMID: 31062216
  28. DIURNAL CYCLE OF HEAT RESISTANCE IN PLANTS.
    Science. 1939 Jun 16;89(2320):556-7 PMID: 17741469
  29. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes.
    Plant J. 2004 Mar;37(6):914-39 PMID: 14996223
  30. PIF4 and ELF3 Act Independently in Arabidopsis thaliana Thermoresponsive Flowering.
    PLoS One. 2016 Aug 26;11(8):e0161791 PMID: 27564448
  31. Natural variants of ELF3 affect thermomorphogenesis by transcriptionally modulating PIF4-dependent auxin response genes.
    BMC Plant Biol. 2015 Aug 14;15:197 PMID: 26269119
  32. Deciphering and prediction of transcriptome dynamics under fluctuating field conditions.
    Cell. 2012 Dec 7;151(6):1358-69 PMID: 23217716
  33. Source-sink dynamics and proteomic reprogramming under elevated night temperature and their impact on rice yield and grain quality.
    New Phytol. 2013 Feb;197(3):825-837 PMID: 23252708
  34. EGRINs (Environmental Gene Regulatory Influence Networks) in Rice That Function in the Response to Water Deficit, High Temperature, and Agricultural Environments.
    Plant Cell. 2016 Oct;28(10):2365-2384 PMID: 27655842
  35. Characterization of the rice circadian clock-associated pseudo-response regulators in Arabidopsis thaliana.
    Biosci Biotechnol Biochem. 2007 Apr;71(4):1107-10 PMID: 17420570
  36. Two Arabidopsis circadian oscillators can be distinguished by differential temperature sensitivity.
    Proc Natl Acad Sci U S A. 2003 May 27;100(11):6878-83 PMID: 12736379
  37. THE ROLE OF NIGHT TEMPERATURE IN PLANT PERFORMANCE.
    Science. 1943 Sep 17;98(2542):265 PMID: 17838677
  38. Neglecting rice milling yield and quality underestimates economic losses from high-temperature stress.
    PLoS One. 2013 Aug 22;8(8):e72157 PMID: 23991056
  39. The transcriptional regulator BBX24 impairs DELLA activity to promote shade avoidance in Arabidopsis thaliana.
    Nat Commun. 2015 Feb 06;6:6202 PMID: 25656233
  40. Photoreceptor effects on plant biomass, resource allocation, and metabolic state.
    Proc Natl Acad Sci U S A. 2016 Jul 5;113(27):7667-72 PMID: 27330114
  41. Different effects of night versus day high temperature on rice quality and accumulation profiling of rice grain proteins during grain filling.
    Plant Cell Rep. 2011 Sep;30(9):1641-59 PMID: 21556707
  42. Rice yields in tropical/subtropical Asia exhibit large but opposing sensitivities to minimum and maximum temperatures.
    Proc Natl Acad Sci U S A. 2010 Aug 17;107(33):14562-7 PMID: 20696908
  43. Global profiling of rice and poplar transcriptomes highlights key conserved circadian-controlled pathways and cis-regulatory modules.
    PLoS One. 2011;6(6):e16907 PMID: 21694767
  44. Circos: an information aesthetic for comparative genomics.
    Genome Res. 2009 Sep;19(9):1639-45 PMID: 19541911
  45. Evidence for the adaptive significance of circadian rhythms.
    Ecol Lett. 2009 Sep;12(9):970-81 PMID: 19566794
  46. The BBX family of plant transcription factors.
    Trends Plant Sci. 2014 Jul;19(7):460-70 PMID: 24582145
  47. Rice responses to rising temperatures--challenges, perspectives and future directions.
    Plant Cell Environ. 2015 Sep;38(9):1686-98 PMID: 25142172
  48. PIF4 Integrates Multiple Environmental and Hormonal Signals for Plant Growth Regulation in Arabidopsis.
    Mol Cells. 2016 Aug 31;39(8):587-93 PMID: 27432188
  49. Transcriptional networks-crops, clocks, and abiotic stress.
    Curr Opin Plant Biol. 2015 Apr;24:39-46 PMID: 25646668
  50. Ambient temperature signal feeds into the circadian clock transcriptional circuitry through the EC night-time repressor in Arabidopsis thaliana.
    Plant Cell Physiol. 2014 May;55(5):958-76 PMID: 24500967
  51. Circadian clock-associated 1 and late elongated hypocotyl regulate expression of the C-repeat binding factor (CBF) pathway in Arabidopsis.
    Proc Natl Acad Sci U S A. 2011 Apr 26;108(17):7241-6 PMID: 21471455
  52. Correlations between Circadian Rhythms and Growth in Challenging Environments.
    Plant Physiol. 2017 Mar;173(3):1724-1734 PMID: 28153924
  53. High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4.
    Curr Biol. 2009 Mar 10;19(5):408-13 PMID: 19249207
  54. CIRCADIAN CLOCK-ASSOCIATED 1 regulates ROS homeostasis and oxidative stress responses.
    Proc Natl Acad Sci U S A. 2012 Oct 16;109(42):17129-34 PMID: 23027948
  55. Phytochromes function as thermosensors in Arabidopsis.
    Science. 2016 Nov 18;354(6314):886-889 PMID: 27789797
  56. Daylength and circadian effects on starch degradation and maltose metabolism.
    Plant Physiol. 2005 Aug;138(4):2280-91 PMID: 16055686
  57. Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage.
    Science. 2005 Jul 22;309(5734):630-3 PMID: 16040710
  58. Phytochrome B integrates light and temperature signals in Arabidopsis.
    Science. 2016 Nov 18;354(6314):897-900 PMID: 27789798
  59. Plant circadian rhythms.
    Plant Cell. 2006 Apr;18(4):792-803 PMID: 16595397
  60. Carbon balance and source-sink metabolic changes in winter wheat exposed to high night-time temperature.
    Plant Cell Environ. 2019 Apr;42(4):1233-1246 PMID: 30471235
  61. RiceXPro version 3.0: expanding the informatics resource for rice transcriptome.
    Nucleic Acids Res. 2013 Jan;41(Database issue):D1206-13 PMID: 23180765
  62. Night temperature has a minimal effect on respiration and growth in rapidly growing plants.
    Ann Bot. 2004 Jul;94(1):155-66 PMID: 15159217
  63. Circadian clocks and adaptation in Arabidopsis.
    Mol Ecol. 2011 Mar;20(6):1155-65 PMID: 21232073
  64. Jasmonate signalling drives time-of-day differences in susceptibility of Arabidopsis to the fungal pathogen Botrytis cinerea.
    Plant J. 2015 Dec;84(5):937-48 PMID: 26466558
  65. JTK_CYCLE: an efficient nonparametric algorithm for detecting rhythmic components in genome-scale data sets.
    J Biol Rhythms. 2010 Oct;25(5):372-80 PMID: 20876817
  66. qEMF3, a novel QTL for the early-morning flowering trait from wild rice, Oryza officinalis, to mitigate heat stress damage at flowering in rice, O. sativa.
    J Exp Bot. 2015 Mar;66(5):1227-36 PMID: 25534925
  67. The B-box family gene STO (BBX24) in Arabidopsis thaliana regulates flowering time in different pathways.
    PLoS One. 2014 Feb 03;9(2):e87544 PMID: 24498334
  68. Ehd4 encodes a novel and Oryza-genus-specific regulator of photoperiodic flowering in rice.
    PLoS Genet. 2013;9(2):e1003281 PMID: 23437005
  69. High night temperature decreases leaf photosynthesis and pollen function in grain sorghum.
    Funct Plant Biol. 2011 Dec;38(12):993-1003 PMID: 32480957
  70. Abiotic stress and the plant circadian clock.
    Plant Signal Behav. 2011 Feb;6(2):223-31 PMID: 21325898
  71. Effect of carbohydrates and night temperature on night respiration in rice.
    J Exp Bot. 2015 Jul;66(13):3931-44 PMID: 25954047
  72. High night temperature strongly impacts TCA cycle, amino acid and polyamine biosynthetic pathways in rice in a sensitivity-dependent manner.
    J Exp Bot. 2015 Oct;66(20):6385-97 PMID: 26208642
  73. A prion-like domain in ELF3 functions as a thermosensor in Arabidopsis.
    Nature. 2020 Sep;585(7824):256-260 PMID: 32848244
  74. Vernalization and Floral Transition in Autumn Drive Winter Annual Life History in Oilseed Rape.
    Curr Biol. 2019 Dec 16;29(24):4300-4306.e2 PMID: 31813609
  75. TOC1-PIF4 interaction mediates the circadian gating of thermoresponsive growth in Arabidopsis.
    Nat Commun. 2016 Dec 14;7:13692 PMID: 27966533
  76. Continuous dynamic adjustment of the plant circadian oscillator.
    Nat Commun. 2019 Feb 1;10(1):550 PMID: 30710080
  77. The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth.
    Nature. 2011 Jul 13;475(7356):398-402 PMID: 21753751
  78. Circadian-associated rice pseudo response regulators (OsPRRs): insight into the control of flowering time.
    Biosci Biotechnol Biochem. 2005 Feb;69(2):410-4 PMID: 15725670
  79. High night temperature induces contrasting responses for spikelet fertility, spikelet tissue temperature, flowering characteristics and grain quality in rice.
    Funct Plant Biol. 2015 Feb;42(2):149-161 PMID: 32480661
  80. STRESSing the role of the plant circadian clock.
    Trends Plant Sci. 2015 Apr;20(4):230-7 PMID: 25631123
  81. Post-flowering night respiration and altered sink activity account for high night temperature-induced grain yield and quality loss in rice (Oryza sativa L.).
    Physiol Plant. 2017 Jan;159(1):59-73 PMID: 27513992
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
DOI
10.1073/pnas.2025899118
Email
kjagadish@ksu.edu
colleen_doherty@ncsu.edu
Published
2021-00-22
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC8237568
Subset
IM
External Links
PubMed source DOI: 10.1073/pnas.2025899118 PMC Full Text View journal details
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