The Role of Phytochromes in Triggering Plant Developmental Transitions

Abstract

Light is an essential stimulus for energy production, plant growth, development and adaptation to constantly changing environmental conditions. Plants sense different wavelengths of light through the action of specialised families of photoreceptor proteins. The molecular and physiological role of the phytochrome family of red/far‐red light receptors is well characterised. Upon light activation, phytochromes trigger multicomponent signalling cascades to induce fundamental cellular processes ranging from gene expression to protein abundance and nuclear architecture to regulate various aspects of plant development. Phytochrome responses are cell autonomous but in some cases mediate interorgan communication to control major developmental and adaptive responses such as flowering initiation and shade avoidance. Reciprocal interactions and integration between phytochrome and circadian signalling pathways are essential for optimising growth and reproductive success during the life cycle of the model plant Arabidopsis thaliana.

Key Concepts

  • Light is a vital informational signal for plant survival and growth.
  • The phytochrome family of plant photoreceptors acts as molecular photoswitches in response to red and far‐red light.
  • Plant phytochrome signal transduction regulates molecular and cellular processes.
  • Phytochromes induce cell‐autonomous responses and interorgan communication.
  • Phytochromes regulate light‐induced developmental transitions as well as adaptation to growth under dense canopy.
  • Plant phytochromes have antagonistic and synergistic roles in regulating photoperiodic flowering in Arabidopsis.
  • Phytochromes inform the endogenous clock about seasonal and daily changes to optimise plant growth and establish reproductive success.

Keywords: light; photoreceptors; phytochromes; development; photomorphogenesis; shade avoidance; flowering; signal integration

Figure 1. (a) Domain composition of plant phytochromes. The amino‐terminal photosensing region consists of a PAS‐like domain, a GAF domain that covalently binds the chromophore phytochromobilin and a PHY‐to‐chrome‐specific domain. The carboxy‐terminal regulatory region consists of two PAS domains and a Histidine‐related kinase domain. (b) Molecular and physiological functions of plant phytochromes. Phytochromes actively regulate a series of cellular processes in response to red and far‐red light and play major roles in inducing major developmental transitions and adaptive responses to red/far‐red light.
Figure 2. Phytochromes are photoswitchable molecules. (a) Plant phytochromes exist in two photoreversible states: Pr absorbs red light and Pfr absorbs far‐red light. (b) Red light induces rapid nuclear translocation of phytochromes in Arabidopsis. Photoactivated phytochromes concentrate in subnuclear domains also known as photobodies.
Figure 3. Phytochromes regulate major aspects of plant development and physiology: (a) seed germination, (b) photomorphogenesis, (c) stomatal opening and development, (d) entrainment of the clock, (e) photoperiodic flowering and (f) shade avoidance response.
Figure 4. Signal transduction pathway mediating the shade avoidance response. R:FR light is perceived in the cotyledons primarily by phyB. PhyB (Pfr) dissociates from PIFs. Accumulation of PIFs leads to induction of YUCCA expression that triggers auxin biosynthesis. Newly synthesised auxin translocates to other organs to promote their elongation.
Figure 5. Photoperiodic control of flowering initiation. (a) Light and endogenous rhythms regulate CONSTANS protein levels. In the dark, the COP1/SPA complex mediates CO degradation. PhyA protects CO from proteasomal degradation. PhyB targets CO for degradation and also induces CO gene expression. Cryptochromes and FKF1 clock receptor stabilise CO protein abundance. Accumulation of CO induces FT expression in plant leaves. (b) FT travels from leaves to the shoot apical meristem (SAM) to initiate flowering by activating the expression of floral development genes, such as AP1. Collectively, red/far‐red and blue light receptors act cooperatively and antagonistically to induce flowering initiation at the optimal time.
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References

Al‐Sady B , Ni W , Kircher S , Schafer E and Quail PH (2006) Photoactivated phytochrome induces rapid PIF3 phosphorylation prior to proteasome‐mediated degradation. Molecular Cell 23: 439–446.

Andres F and Coupland G (2012) The genetic basis of flowering responses to seasonal cues. Nature Reviews. Genetics 13: 627–639.

Bourbousse C , Mestiri I , Zabulon G , et al. (2015) Light signaling controls nuclear architecture reorganisation during seedling establishment. Proceedings of the National Academy of Sciences of the United States of America 112: E2836–E2844.

Briggs WR and Christie JM (2002) Phototropins 1 and 2: versatile plant blue‐light receptors. Trends in Plant Science 7: 204–210.

Brown BA , Cloix C , Jiang GH , et al. (2005) A UV‐B‐specific signaling component orchestrates plant UV protection. Proceedings of the National Academy of Sciences of the United States of America 102: 18225–18230.

Casal JJ and Smith H (1988) The loci of perception for phytochrome control of internode growth in light‐grown mustard: Promotion by low phytochrome photoequilibria in the internode is enhanced by blue light perceived by the leaves. Planta 176: 277–282.

Casal JJ (2013) Photoreceptor signaling networks in plant responses to shade. Annual Review of Plant Biology 64: 403–427. DOI: 10.1146/annurev-arplant-050312-120221.

Casson SA , Franklin KA , Gray JE , et al. (2009) phytochrome B and PIF4 regulate stomatal development in response to light quantity. Current Biology 19: 229–234.

Casson SA and Hetherington AM (2014) phytochrome B Is required for light‐mediated systemic control of stomatal development. Current Biology 24: 1216–1221.

Cerdan PD and Chory J (2003) Regulation of flowering time by light quality. Nature 423: 881–885.

Chen M and Chory J (2011) Phytochrome signaling mechanisms and the control of plant development. Trends in Cell Biology 21 (11): 664–671. DOI: 10.1016/j.tcb.2011.07.002.

Chen F , Li B , Li G , et al. (2014) Arabidopsis phytochrome A directly targets numerous promoters for individualized modulation of genes in a wide range of pathways. The Plant Cell 26: 1949–1966.

Christie JM , Blackwood L , Petersen J and Sullivan S (2015) Plant flavoprotein photoreceptors. Plant & Cell Physiology 56: 401–413.

Devlin PF , Yanovsky MJ and Kay SA (2003) A genomic analysis of the shade avoidance response in Arabidopsis . Plant Physiology 133: 1617–1629.

Doherty CJ and Kay SA (2010) Circadian control of global gene expression patterns. Annual Review of Genetics 44: 419–444.

Donohue K , Heschel MS , Butler CM , et al. (2008) Diversification of phytochrome contributions to germination as a function of seed‐maturation environment. The New Phytologist 177: 367–379.

Endo M , Nakamura S , Araki T , Mochizuki N and Nagatani A (2005) Phytochrome B in the mesophyll delays flowering by suppressing FLOWERING LOCUS T expression in Arabidopsis vascular bundles. The Plant Cell 17: 1941–1952.

Endo M , Tanigawa Y , Murakami T , Araki T and Nagatani A (2013) Phytochrome‐dependent late‐flowering accelerates flowering through physical interactions with phytochrome B and CONSTANS. Proceedings of the National Academy of Sciences of the United States of America 110: 18017–18022.

Feng CM , Qiu Y , Van Buskirk EK , Yang EJ and Chen M (2014) Light‐regulated gene repositioning in Arabidopsis . Nature Communications 5: 3027.

Franklin KA and Quail PH (2010) Phytochrome functions in Arabidopsis development. Journal of Experimental Botany 61 (1): 11–24. DOI: 10.1093/jxb/erp304.

Greenham K and McClung CR (2015) Integrating circadian dynamics with physiological processes in plants. Nature Reviews. Genetics 16: 598–610.

Heijde M and Ulm R (2012) UV‐B photoreceptor‐mediated signalling in plants. Trends in Plant Science 17: 230–237.

Hennig L , Stoddart WM , Dieterle M , Whitelam GC and Schafer E (2002) Phytochrome E controls light‐induced germination of Arabidopsis . Plant Physiology 128: 194–200.

Hsu PY and Harmer SL (2014) Wheels within wheels: the plant circadian system. Trends in Plant Science 19: 240–249.

Huang H , Alvarez S , Bindbeutel RK , et al. (2016) Identification of evening complex associated proteins in Arabidopsis by affinity purification and mass spectrometry. Molecular & Cellular Proteomics 15 (1): 201–217. DOI: 10.1074/mcp.M115.054064.

Inigo S , Giraldez AN , Chory J and Cerdan PD (2012) Proteasome‐mediated turnover of Arabidopsis MED25 is coupled to the activation of FLOWERING LOCUS T transcription. Plant Physiology 160: 1662–1673.

Ito S , Song YH , Josephson‐Day AR , et al. (2012) FLOWERING BHLH transcriptional activators control expression of the photoperiodic flowering regulator CONSTANS in Arabidopsis . Proceedings of the National Academy of Sciences of the United States of America 109: 3582–3587.

Jang S , Marchal V , Panigrahi KC , et al. (2008) Arabidopsis COP1 shapes the temporal pattern of CO accumulation conferring a photoperiodic flowering response. The EMBO Journal 27: 1277–1288.

Jang IC , Henriques R , Seo HS , Nagatani A and Chua NH (2010) Arabidopsis phytochrome interacting factor proteins promote phytochrome B polyubiquitination by COP1 E3 ligase in the nucleus. The Plant Cell 22: 2370–2383.

Johansson M and Staiger D (2015) Time to flower: interplay between photoperiod and the circadian clock. Journal of Experimental Botany 66 (3): 719–730. DOI: 10.1093/jxb/eru441.

Kaiserli E , Paldi K , O'Donnell L , et al. (2015) Integration of light and photoperiodic signaling in transcriptional nuclear foci. Developmental Cell 35: 311–321.

Keller MM , Jaillais Y , Pedmale UV , et al. (2011) Cryptochrome 1 and phytochrome B control shade‐avoidance responses in Arabidopsis via partially independent hormonal cascades. The Plant Journal: For Cell and Molecular Biology 67: 195–207.

Keuskamp DH , Pollmann S , Voesenek LA , Peeters AJ and Pierik R (2010) Auxin transport through PIN‐FORMED 3 (PIN3) controls shade avoidance and fitness during competition. Proceedings of the National Academy of Sciences of the United States of America 107: 22740–22744.

Kevei E , Schafer E and Nagy F (2007) Light‐regulated nucleo‐cytoplasmic partitioning of phytochromes. Journal of Experimental Botany 58: 3113–3124.

Kircher S , Kozma‐Bognar L , Kim L , et al. (1999) Light quality‐dependent nuclear import of the plant photoreceptors phytochrome A and B. The Plant Cell 11: 1445–1456.

Lazaro A , Valverde F , Pineiro M and Jarillo JA (2012) The Arabidopsis E3 ubiquitin ligase HOS1 negatively regulates CONSTANS abundance in the photoperiodic control of flowering. The Plant Cell 24: 982–999.

Leivar P and Quail PH (2011) PIFs: pivotal components in a cellular signaling hub. Trends in Plant Science 16: 19–28.

Leivar P , Tepperman JM , Cohn MM , et al. (2012) Dynamic antagonism between phytochromes and PIF family basic helix‐loop‐helix factors induces selective reciprocal responses to light and shade in a rapidly responsive transcriptional network in Arabidopsis . The Plant Cell 24: 1398–1419.

Li L , Ljung K , Breton G , et al. (2012) Linking photoreceptor excitation to changes in plant architecture. Genes & Development 26: 785–790.

Lin C (2000) Photoreceptors and regulation of flowering time. Plant Physiology 123: 39–50.

Liu XL , Covington MF , Fankhauser C , Chory J and Wagner DR (2001) ELF3 encodes a circadian clock‐regulated nuclear protein that functions in an Arabidopsis PHYB signal transduction pathway. The Plant Cell 13: 1293–1304.

Liu H , Liu B , Zhao C , Pepper M and Lin C (2011) The action mechanisms of plant cryptochromes. Trends in Plant Science 16: 684–691.

Loudet O , Michael TP , Burger BT , et al. (2008) A zinc knuckle protein that negatively controls morning‐specific growth in Arabidopsis thaliana . Proceedings of the National Academy of Sciences of the United States of America 105: 17193–17198.

Martinez‐Garcia JF , Huq E and Quail PH (2000) Direct targeting of light signals to a promoter element‐bound transcription factor. Science 288: 859–863.

Medzihradszky M , Bindics J , Adam E , et al. (2013) Phosphorylation of phytochrome B inhibits light‐induced signaling via accelerated dark reversion in Arabidopsis . The Plant Cell 25: 535–544.

Millar AJ (2003) A suite of photoreceptors entrains the plant circadian clock. Journal of Biological Rhythms 18: 217–226.

Nagatani A (2010) Phytochrome: structural basis for its functions. Current Opinion in Plant Biology 13: 565–570.

Ni W , Xu SL , Tepperman JM , et al. (2014) A mutually assured destruction mechanism attenuates light signaling in Arabidopsis . Science 344: 1160–1164.

Nieto C , Lopez‐Salmeron V , Daviere JM and Prat S (2015) ELF3‐PIF4 interaction regulates plant growth independently of the evening complex. Current Biology 25: 187–193.

Nito K , Wong CC , Yates JR 3rd and Chory J (2013) Tyrosine phosphorylation regulates the activity of phytochrome photoreceptors. Cell Reports 3: 1970–1979.

Nito K , Kajiyama T , Unten‐Kobayashi J , et al. (2015) Spatial regulation of the gene expression response to shade in Arabidopsis seedlings. Plant & Cell Physiology 56: 1306–1319.

Nozue K , Covington MF , Duek PD , et al. (2007) Rhythmic growth explained by coincidence between internal and external cues. Nature 448: 358–361.

Nusinow DA , Helfer A , Hamilton EE , et al. (2011) The ELF4‐ELF3‐LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature 475: 398–402.

Osterlund MT , Hardtke CS , Wei N and Deng XW (2000) Targeted destabilisation of HY5 during light‐regulated development of Arabidopsis . Nature 405: 462–466.

Possart A , Fleck C and Hiltbrunner A (2014) Shedding (far‐red) light on phytochrome mechanisms and responses in land plants. Plant Science: An International Journal of Experimental Plant Biology 217–218: 36–46.

Procko C , Crenshaw CM , Ljung K , Noel JP and Chory J (2014) Cotyledon‐generated auxin is required for shade‐induced hypocotyl growth in Brassica rapa . Plant Physiology 165: 1285–1301.

Quail PH (2002) Phytochrome photosensory signalling networks. Nature Reviews. Molecular Cell Biology 3: 85–93.

Sadanandom A , Adam E , Orosa B , et al. (2015) SUMOylation of phytochrome‐B negatively regulates light‐induced signaling in Arabidopsis thaliana . Proceedings of the National Academy of Sciences of the United States of America 112: 11108–11113.

Seo HS , Watanabe E , Tokutomi S , Nagatani A and Chua NH (2004) Photoreceptor ubiquitination by COP1 E3 ligase desensitizes phytochrome A signaling. Genes & Development 18: 617–622.

Shimazaki K , Doi M , Assmann SM and Kinoshita T (2007) Light regulation of stomatal movement. Annual Review of Plant Biology 58: 219–247.

Shinomura T , Nagatani A , Hanzawa H , et al. (1996) Action spectra for phytochrome A‐ and B‐specific photoinduction of seed germination in Arabidopsis thaliana . Proceedings of the National Academy of Sciences of the United States of America 93: 8129–8133.

Smith H , Xu Y and Quail PH (1997) Antagonistic but complementary actions of phytochromes A and B allow seedling de‐etiolation. Plant Physiology 114: 637–641.

Song YH , Shim JS , Kinmonth‐Schultz HA and Imaizumi T (2015) Photoperiodic flowering: time measurement mechanisms in leaves. Annual Review of Plant Biology 66: 441–464.

Su YS and Lagarias JC (2007) Light‐independent phytochrome signaling mediated by dominant GAF domain tyrosine mutants of Arabidopsis phytochromes in transgenic plants. The Plant Cell 19: 2124–2139.

Tanaka S , Nakamura S , Mochizuki N and Nagatani A (2002) Phytochrome in cotyledons regulates the expression of genes in the hypocotyl through auxin‐dependent and ‐independent pathways. Plant & Cell Physiology 43: 1171–1181.

Tao Y , Ferrer JL , Ljung K , et al. (2008) Rapid synthesis of auxin via a new tryptophan‐dependent pathway is required for shade avoidance in plants. Cell 133: 164–176.

Toth R , Kevei E , Hall A , et al. (2001) Circadian clock‐regulated expression of phytochrome and cryptochrome genes in Arabidopsis . Plant Physiology 127: 1607–1616.

Turck F , Fornara F and Coupland G (2008) Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annual Review of Plant Biology 59: 573–594.

Valverde F , Mouradov A , Soppe W , et al. (2004) Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303: 1003–1006.

Van Buskirk EK , Decker PV and Chen M (2012) Photobodies in light signaling. Plant Physiology 158: 52–60.

Wang H and Wang H (2015) Phytochrome signaling: time to tighten up the loose ends. Molecular Plant 8 (4): 540–551. DOI: 10.1016/j.molp.2014.11.021.

Weitzman M and Hahn KM (2014) Optogenetic approaches to cell migration and beyond. Current Opinion in Cell Biology 30: 112–120.

Xu X , Paik I , Zhu L and Huq E (2015) Illuminating progress in phytochrome‐mediated light signaling pathways. Trends in Plant Science 20: 641–650.

Yanovsky MJ and Kay SA (2002) Molecular basis of seasonal time measurement in Arabidopsis . Nature 419: 308–312.

Yasui Y , Mukougawa K , Uemoto M , et al. (2012) The phytochrome‐interacting vascular plant one‐zinc finger1 and VOZ2 redundantly regulate flowering in Arabidopsis . The Plant Cell 24: 3248–3263.

van Zanten M , Tessadori F , Peeters AJ and Fransz P (2012) Shedding light on large‐scale chromatin reorganisation in Arabidopsis thaliana . Molecular Plant 5: 583–590.

Further Reading

Shim JS and Imaizumi T (2015) Circadian clock and photoperiodic response in Arabidopsis: From seasonal flowering to redox homeostasis. Biochemistry 54 (2): 157–170. DOI: 10.1021/bi500922q.

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Kaiserli, Eirini, and Chory, Joanne(Mar 2016) The Role of Phytochromes in Triggering Plant Developmental Transitions. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0023714]