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The phytochrome-interacting family of transcription factors in maize (Zea mays L.): identification, evolution, and expression analysis

  • Yong GaoEmail author
  • Xiaoyun Ren
  • Jingjie Qian
  • Qian Li
  • Haixia Tao
  • Jianmin ChenEmail author
Short Communication

Abstract

The phytochrome-interacting factor (PIF) subfamily of transcription factors is among the most important families of plant transcriptional regulators. PIFs regulate multiple biological processes, especially the photomorphogenic development. However, studies on PIF are mostly concentrated in Arabidopsis, little information on PIFs in maize (Zea mays L.) is currently available. The release of assembled genome sequences of maize enables the genome-wide investigation of maize PIF proteins. In this study, six PIF genes in maize were identified and named ZmPIF16. Among them, ZmPIF1 and ZmPIF3 were previously cloned in our laboratory. According to the structural features of their proteins, maize PIF genes (ZmPIFs) were classified into two main groups. Group I have an active phytochrome B (APB) domain and interacts with ZmphyB1. Group II has APA and APB domains and interacts with ZmphyA1 and ZmphyB1. The global expression patterns of ZmPIF genes in various tissues, as well as response of ZmPIF genes to diurnal rhythm, environmental stresses, and plant hormones were analyzed. The expression patterns of the ZmPIF genes suggested that ZmPIF1 and ZmPIF3 play an important role in the diurnal rhythm, while ZmPIF4 and ZmPIF6 are possibly the genes that respond to stimulation during plant growth and development. Meanwhile, the functions of ZmPIF2 and ZmPIF5 requires further investigation. These results can facilitate the exploration of the role of maize PIF-mediated plant signaling pathways and contribute to the development of molecular breeding for maize.

Keywords

PIF Maize Phytochrome Stresses Plant hormones 

Abbreviations

PIF

Phytochrome-interacting factor

bHLH

Basic/helix-loop-helix

APB

Active phytochrome B-binding

APA

Active phytochrome A-binding

ABA

Abscisic acid

GA

Gibberellin

BR

Brassinosteroid

JA

Jasmonate

ORF

Open reading frame

Notes

Acknowledgements

This work was supported by the National Natural Science Foundation of China (no. 31771686); the Natural Science Foundation of Jiangsu Province (no. BK20161334); State Key Laboratory of Crop Biology (no. 2016KF03); Priority Academic Program Development of Jiangsu Higher Education Institutions and State Key Laboratory of Crop Biology.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11738_2018_2802_MOESM1_ESM.pdf (14 kb)
Supplementary material 1 (PDF 15 KB)

References

  1. Bai MY, Shang JX, Oh E, Fan M, Bai Y, Zentella R, Sun TP, Wang ZY (2012) Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat Cell Biol 14:810–817CrossRefGoogle Scholar
  2. Castillon A, Shen H, Huq E (2007) Phytochrome interacting factors: central players in phytochrome-mediated light signaling networks. Trends Plant Sci 12:514–521CrossRefGoogle Scholar
  3. Clack T, Shokry A, Moffet M, Liu P, Faul M, Sharrock RA (2009) Obligate heterodimerization of Arabidopsis phytochromes C and E and interaction with the PIF3 basic helix-loop-helix transcription factor. Plant Cell 21:786–799CrossRefGoogle Scholar
  4. de Lucas M, Prat S (2014) PIFs get BRright: PHYTOCHROME INTERACTING FACTORs as integrators of light and hormonal signals. New Phytol 202:1126–1141CrossRefGoogle Scholar
  5. de Lucas M, Daviere JM, Rodriguez-Falcon M, Pontin M, Iglesias-Pedraz JM, Lorrain S, Fankhauser C, Blazquez MA, Titarenko E, Prat S (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451:480–484CrossRefGoogle Scholar
  6. Feng SH, Martinez C, Gusmaroli G et al (2008) Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451:475–479CrossRefGoogle Scholar
  7. Gao Y, Jiang W, Dai Y, Xiao N, Zhang CQ, Li H, Lu Y, Wu MQ, Tao XY, Deng DX, Chen JM (2015) A maize phytochrome-interacting factor 3 improves drought and salt stress tolerance in rice. Plant Mol Biol 87:413–428CrossRefGoogle Scholar
  8. Gao Y, Wu MQ, Zhang MJ, Jiang W, Liang EX, Zhang DP, Zhang CQ, Xiao N, Chen JM (2018a) Roles of a maize phytochrome-interacting factors protein ZmPIF3 in regulation of drought stress responses by controlling stomatal closure in transgenic rice without yield penalty. Plant Mol Biol.  https://doi.org/10.1007/s11103-018-0739-4 CrossRefPubMedGoogle Scholar
  9. Gao Y, Wu MQ, Zhang MJ, Jiang W, Ren XY, Liang EX, Zhang DP, Zhang CQ, Xiao N, Li Y, Dai Y, Chen JM (2018b) A maize phytochrome-interacting factors protein ZmPIF1 enhances drought tolerance by inducing stomatal closure and improves grain yield in Oryza sativa. Plant Biotechnol J 16:1375–1387CrossRefGoogle Scholar
  10. Hornitschek P, Kohnen MV, Lorrain S et al (2012) Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling. Plant J 71:699–711CrossRefGoogle Scholar
  11. Huq E, Quail PH (2002) PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis. EMBO J 21:2441–2450CrossRefGoogle Scholar
  12. Jin JP, Tian F, Yang DC, Meng YQ, Kong L, Luo JC, Gao G (2017) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res 45:D1040–D1045CrossRefGoogle Scholar
  13. Khanna R, Huq E, Kikis EA, Al-Sady B, Lanzatella C, Quail PH (2004) A novel molecular recognition motif necessary for targeting photoactivated phytochrome signaling to specific basic helix-loop-helix transcription factors. Plant Cell 16:3033–3044CrossRefGoogle Scholar
  14. Kim DH, Yamaguchi S, Lim S, Oh E, Park J, Hanada A, Kamiya Y, Choi G (2008) SOMNUS, a CCCH-type zinc finger protein in Arabidopsis, negatively regulates light-dependent seed germination downstream of PIL5. Plant Cell 20:1260–1277CrossRefGoogle Scholar
  15. Kim K, Shin J, Lee SH, Kweon HS, Maloof JN, Choi G (2011) Phytochromes inhibit hypocotyl negative gravitropism by regulating the development of endodermal amyloplasts through phytochrome-interacting factors. Proc Natl Acad Sci USA 108:1729–1734CrossRefGoogle Scholar
  16. Kim J, Kang H, Park J, Kim W, Yoo J, Lee N, Kim J, Choi G (2016) PIF1-interacting transcription factors and their binding sequence elements determine the in vivo targeting sites of PIF1. Plant Cell 28:1388–1405CrossRefGoogle Scholar
  17. Koini MA, Alvey L, Allen T, Tilley CA, Harberd NP, Whitelam GC, Franklin KA (2009) High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr Biol 19:408–413CrossRefGoogle Scholar
  18. Kudo M, Kidokoro S, Yoshida T, Mizoi J, Todaka D, Fernie AR, Shinozaki K, Yamaguchi-Shinozaki K (2016) Double overexpression of DREB and PIF transcription factors improves drought stress tolerance and cell elongation in transgenic plants. Plant Biotechnol J 15:458–471CrossRefGoogle Scholar
  19. Kumar I, Swaminathan K, Hudson K, Hudson ME (2016) Evolutionary divergence of phytochrome protein function in Zea mays PIF3 signaling. J Exp Bot 67:4231–4240CrossRefGoogle Scholar
  20. Ledent V, Vervoort M (2001) The basic helix-loop-helix protein family:comparative genomics and phylogenetic analysis. Genome Res 11:754–770CrossRefGoogle Scholar
  21. Leivar P, Monte E (2014) PIFs: systems integrators in plant development. Plant Cell 26:56–78CrossRefGoogle Scholar
  22. Leivar P, Quail PH (2011) PIFs: pivotal components in a cellular signaling hub. Trends Plant Sci 16:19–28CrossRefGoogle Scholar
  23. Leivar P, Tepperman JM, Cohn MM, Monte E, Al-Sady B, Erickson E, Quail PH (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. Plant Cell 24:1398–1419CrossRefGoogle Scholar
  24. Li XX, Duan XP, Jiang HX et al (2006) Genome-wide analysis of basic/helix-loop-helix transcription factor family in rice and Arabidopsis. Plant Physiol 141:1167–1184CrossRefGoogle Scholar
  25. Ni M, Tepperman JM, Quail PH (1998) PIF3, a phytochrome-interacting factor necessary for normal photoinduced signal transduction, is a novel basic helix-loop-helix protein. Cell 95:657–667CrossRefGoogle Scholar
  26. Ni WM, Xu SL, Gonzalez-Grandio E, Chalkley RJ, Huhmer AFR, Burlingame AL, Wang ZY, Quail PH (2017) PPKs mediate direct signal transfer from phytochrome photoreceptors to transcription factor PIF3. Nat Commun 8:15236CrossRefGoogle Scholar
  27. Oh E, Kim J, Park E, Kim JI, Kang C, Choi G (2004) PIL5, a phytochrome-interacting basic helix-loop-helix protein, is a key negative regulator of seed germination in Arabidopsis thaliana. Plant Cell 16:3045–3058CrossRefGoogle Scholar
  28. Oh E, Yamaguchi S, Hu JH, Yusuke J, Jung B, Paik I, Lee HS, Sun TP, Kamiya Y, Choi G (2007) PIL5, a phytochrome-interacting bHLH protein, regulates gibberellin responsiveness by binding directly to the GAI and RGA promoters in Arabidopsis seeds. Plant Cell 19:1192–1208CrossRefGoogle Scholar
  29. Oh E, Kang H, Yamaguchi S, Park J, Lee D, Kamiya Y, Choi G (2009) Genome-wide analysis of genes targeted by PHYTOCHROME INTERACTING FACTOR 3-LIKE5 during seed germination in Arabidopsis. Plant Cell 21:403–419CrossRefGoogle Scholar
  30. Pham VN, Kathare PK, Huq E (2018) Phytochromes and phytochrome interacting factors. Plant Physiol 176:1025–1038CrossRefGoogle Scholar
  31. Quint M, Delker C, Franklin KA, Wigge PA, Halliday KJ, van Zanten M (2016) Molecular and genetic control of plant thermomorphogenesis. Nat Plants 2:15190CrossRefGoogle Scholar
  32. Sakuraba Y, Jeong J, Kang MY, Kim J, Paek NC, Choi G (2014) Phytochrome-interacting transcription factors PIF4 and PIF5 induce leaf senescence in Arabidopsis. Nat Commun 5:4636CrossRefGoogle Scholar
  33. Sheehan MJ, Farmer PR, Brutnell TP (2004) Structure and expression of maize phytochrome family homeologs. Genetics 167:1395–1405CrossRefGoogle Scholar
  34. Shen H, Zhu L, Castillon A, Majee M, Downie B, Huq E (2008) Light-induced phosphorylation and degradation of the negative regulator phytochrome-interacting factor1 from Arabidopsis depend upon its direct physical interactions with photoactivated phytochromes. Plant Cell 20:1586–1602CrossRefGoogle Scholar
  35. Shi QB, Zhang HS, Song XY, Jiang YE, Liang R, Li G (2018) Functional characterization of the maize phytochrome-interacting factors PIF4 and PIF5. Front Plant Sci 8:2273CrossRefGoogle Scholar
  36. Shin J, Kim K, Kang H, Zulfugarov IS, Bae G, Lee CH, Lee D, Choi G (2009) Phytochromes promote seedling light responses by inhibiting four negatively-acting phytochrome interacting factors. Proc Natl Acad Sci USA 106:7660–7665CrossRefGoogle Scholar
  37. Soy J, Leivar P, González-Schain N, Sentandreu M, Prat S, Quail PH, Monte E (2012) Phytochrome-imposed oscillations in PIF3 protein abundance regulate hypocotyl growth under diurnal light/dark conditions in Arabidopsis. Plant J 71:390–401PubMedPubMedCentralGoogle Scholar
  38. Soy J, Leivar P, Gonzalez-Schain N, Martin G, Diaz C, Sentandreu M, Al-Sady B, Quail PH, Monte E (2016) Molecular convergence of clock and photosensory pathways through PIF3-TOC1 interaction and co-occupancy of target promoters. Proc Natl Acad Sci USA 113:4870–4875CrossRefGoogle Scholar
  39. Sun JQ, Qi LL, Li YN, Chu JF, Li CY (2012) PIF4-mediated activation of YUCCA8 expression integrates temperature into the auxin pathway in regulating Arabidopsis hypocotyl growth. PLoS Genet 8:e1002594CrossRefGoogle Scholar
  40. Todaka D, Nakashima K, Maruyama K et al (2012) Rice phytochrome-interacting factor-like protein OsPIL1 functions as a key regulator of internode elongation and induces a morphological response to drought stress. Proc Natl Acad Sci USA 109:15947–15952CrossRefGoogle Scholar
  41. Toledo-Ortiz G, Huq E, Quail PH (2003) The Arabidopsis basic/helixloop-helix transcription factor family. Plant Cell 15:1749–1770CrossRefGoogle Scholar
  42. Yang DL, Yao J, Mei CS et al (2012) Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. Proc Natl Acad Sci USA 109:E1192–E1200CrossRefGoogle Scholar
  43. Zhong S, Shi H, Xue C, Wang L, Xi Y, Li J, Quail PH, Deng XW, Guo H (2012) A molecular framework of light-controlled phytohormone action in Arabidopsis. Curr Biol 22:1530–1535CrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2019

Authors and Affiliations

  1. 1.Jiangsu Key Laboratories of Crop Genetics and Physiology and Plant Functional Genomics of the Ministry of Education, Co-Innovation Center for Modern Production Technology of Grain Crops of Jiangsu ProvinceYangzhou UniversityYangzhouChina

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