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Four HD-ZIPs are involved in banana fruit ripening by activating the transcription of ethylene biosynthetic and cell wall-modifying genes

  • Ying-Ying Yang
  • Wei Shan
  • Jian-Fei Kuang
  • Jian-Ye Chen
  • Wang-Jin LuEmail author
Original Article

Abstract

Key message

Four MaHDZs are possibly involved in banana fruit ripening by activating the transcription of genes related to ethylene biosynthesis and cell wall degradation, such as MaACO5MaEXP2, MaEXPA10, MaPG4 and MaPL4.

Abstract

The homeodomain-leucine zipper (HD-ZIP) proteins represent plant-specific transcription factors, which contribute to various plant physiological processes. However, little information is available regarding the association of HD-ZIPs with banana fruit ripening. In this study, we identified a total of 96 HD-ZIP genes in banana genome, which were divided into four different groups consisting of 35, 31, 9 and 21 members in the I, II, III and IV subfamilies, respectively. The expression patterns of MaHDZ genes during fruit ripening showed that MaHDZI.19, MaHDZI.26, MaHDZII.4 and MaHDZII.7 were significantly up-regulated in the ripening stage and thus suggested to be potential regulators of banana fruit ripening. Furthermore, MaHDZI.19, MaHDZI.26, MaHDZII.4 and MaHDZII.7 were found to localize exclusively in the nucleus and exhibit transcriptional activation capacities. Importantly, MaHDZI.19, MaHDZI.26, MaHDZII.4 and MaHDZII.7 stimulated the transcription of several ripening-related genes including MaACO5 related to ethylene biosynthesis, MaEXP2, MaEXPA10, MaPG4 and MaPL4 were associated with cell wall degradation, through directly binding to their promoters. Taken together, our findings expand the functions of HD-ZIP transcription factors and identify four MaHDZs likely involved in regulating banana fruit ripening by activating the expression of genes related to ethylene biosynthesis and cell wall modification, which may have potential application in banana molecular breeding.

Keywords

Banana HD-ZIP Fruit ripening Transcriptional regulation 

Abbreviations

1-MCP

1-Methylcyclopropene

ACO

1-Aminocyclopropane-1-carboxylate oxidase

EMSA

Electrophroretic mobility shift assay

EXP

Expansin

GFP

Green fluorescent protein

HD-ZIP

Homeodomain-leucine zipper

IPTG

Isopropyl thio-β-d-galactoside

TFs

Transcription factors

Mw

Molecular weight

PG

Polygalacturonase

pI

Isoelectric point

PL

Pectinate lyases

qRT-PCR

Quantitative real-time polymerase chain reaction

X-α-Gal

X-α-galactosidase

Y2H

Yeast two-hybrid

Notes

Acknowledgements

We thank Dr. George P. Lomonossoff (John Innes Centre, Norwich Research Park) for the generous gift of pEAQ vectors. This work was financially supported by the grants from the Natural Science Foundation of China (Grant no. 31830071), and China Agriculture Research System (Grant no. CARS-31-11).

Author contribution statement

YYY performed the experiments, interpreted the results and wrote the article; YYY and WS analyzed the data and performed statistical analyses; JFK and JYC contributed to experiment design and manuscript editing; WJL designed and coordinated the experiments, and revised and improved the manuscript; WJL is responsible for the manuscript as a whole.

Compliance with ethical standards

Conflict of interest

The authors have no conflicts of interest to declare.

Supplementary material

299_2019_2495_MOESM1_ESM.pdf (508 kb)
Supplementary material 1 (PDF 508 kb)

References

  1. Agalou A, Purwantomo S, Övernäs E et al (2008) A genome-wide survey of HD-Zip genes in rice and analysis of drought-responsive family members. Plant Mol Biol 66:87–103PubMedCrossRefPubMedCentralGoogle Scholar
  2. Ariel FD, Manavella PA, Dezar CA, Chan RL (2007) The true story of the HD-Zip family. Trends Plant Sci 12:419–426PubMedCrossRefPubMedCentralGoogle Scholar
  3. Ariel F, Diet A, Verdenaud M et al (2010) Environmental regulation of lateral root emergence in Medicago truncatula requires the HD-Zip I transcription factor HB1. Plant Cell 22:2171–2183PubMedPubMedCentralCrossRefGoogle Scholar
  4. Asif MH, Lakhwani D, Pathak S et al (2014) Transcriptome analysis of ripe and unripe fruit tissue of banana identifies major metabolic networks involved in fruit ripening process. BMC Plant Biol 14:316PubMedPubMedCentralCrossRefGoogle Scholar
  5. Ba LJ, Shan W, Xiao YY et al (2014) A ripening-induced transcription factor MaBSD1 interacts with promoters of MaEXP1/2 from banana fruit. Plant Cell Rep 33:1913–1920PubMedCrossRefPubMedCentralGoogle Scholar
  6. Baima S, Possenti M, Matteucci A et al (2001) The arabidopsis ATHB-8 HD-zip protein acts as a differentiation-promoting transcription factor of the vascular meristems. Plant Physiol 126:643–655PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bang SW, Lee DK, Jung H et al (2018) Overexpression of OsTF1L, a rice HD-Zip transcription factor, promotes lignin biosynthesis and stomatal closure that improves drought tolerance. Plant Biotechnol J 17:118–131PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bartley GE, Ishida BK (2007) Ethylene-sensitive and insensitive regulation of transcription factor expression during in vitro tomato sepal ripening. J Exp Bot 58:2043–2051PubMedCrossRefPubMedCentralGoogle Scholar
  9. Brinker M, Brosché M, Vinocur B et al (2010) Linking the salt transcriptome with physiological responses of a salt-resistant Populus species as a strategy to identify genes important for stress acclimation. Plant Physiol 154:1697–1709PubMedPubMedCentralCrossRefGoogle Scholar
  10. Cabello JV, Arce AL, Chan RL (2015) The homologous HD-Zip I transcription factors HaHB1 and AtHB13 confer cold tolerance via the induction of pathogenesis-related and glucanase proteins. Plant J 69:141–153CrossRefGoogle Scholar
  11. Chen L, Zhong H, Kuang J et al (2011) Validation of reference genes for RT-qPCR studies of gene expression in banana fruit under different experimental conditions. Planta 234:377–390PubMedCrossRefPubMedCentralGoogle Scholar
  12. Chen C, Chen H, He Y, Xia R (2018) TBtools, a Toolkit for Biologists integrating various HTS-data handling tools with a user-friendly interface. BioRxiv.  https://doi.org/10.1101/289660 CrossRefGoogle Scholar
  13. Ciarbelli AR, Ciolfi A, Salvucci S et al (2008) The Arabidopsis Homeodomain-leucine Zipper II gene family: diversity and redundancy. Plant Mol Biol 68:465–478PubMedCrossRefPubMedCentralGoogle Scholar
  14. D’Hont A, Denoeud F, Aury JM et al (2012) The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488:213–217PubMedCrossRefPubMedCentralGoogle Scholar
  15. Emery JF, Floyd SK, Alvarez J et al (2003) Radial patterning of arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr Biol 13:1768–1774PubMedCrossRefPubMedCentralGoogle Scholar
  16. Fan ZQ, Ba LJ, Shan W et al (2018a) A banana R2R3-MYB transcription factor MaMYB3 is involved in fruit ripening through modulation of starch degradation by repressing starch degradation-related genes and MabHLH6. Plant J 96:1191–1205PubMedCrossRefPubMedCentralGoogle Scholar
  17. Fan ZQ, Tan XL, Shan W et al (2018b) Characterization of a transcriptional regulator, BrWRKY6, associated with gibberellin-suppressed leaf senescence of Chinese flowering cabbage. J Agric Food Chem 66:1791–1799PubMedCrossRefPubMedCentralGoogle Scholar
  18. Franco DM, Silva EM, Saldanha LL et al (2015) Flavonoids modify root growth and modulate expression of SHORT-ROOT and HD-ZIP III. J Plant Physiol 188:89–95PubMedCrossRefPubMedCentralGoogle Scholar
  19. Goel R, Pandey A, Trivedi PK, Asif MH (2016) Genome-wide analysis of the Musa WRKY gene family: evolution and differential expression during development and stress. Front Plant Sci 7:299PubMedPubMedCentralCrossRefGoogle Scholar
  20. Green KA, Prigge MJ, Katzman RB, Clark SE (2005) CORONA, a member of the class III homeodomain leucine zipper gene family in arabidopsis, regulates stem cell specification and organogenesis. Plant Cell 17:691–704PubMedPubMedCentralCrossRefGoogle Scholar
  21. Gu C, Guo ZH, Cheng HY et al (2019) A HD-ZIP II HOMEBOX transcription factor, PpHB. G7, mediates ethylene biosynthesis during fruit ripening in peach. Plant Sci 278:12–19PubMedCrossRefPubMedCentralGoogle Scholar
  22. Guo Y, Shan W, Liang S et al (2019) MaBZR1/2 act as transcriptional repressors of ethylene biosynthetic genes in banana fruit. Physiol Plant 165:555–568PubMedCrossRefPubMedCentralGoogle Scholar
  23. Han YC, Fu CC, Kuang JF et al (2016a) Two banana fruit ripening-related C2H2 zinc finger proteins are transcriptional repressors of ethylene biosynthetic genes. Postharvest Biol Technol 116:8–15CrossRefGoogle Scholar
  24. Han YC, Kuang JF, Chen JY et al (2016b) Banana transcription factor MaERF11 recruits histone deacetylase MaHDA1 and represses the expression of MaACO1 and expansins during fruit ripening. Plant Physiol 171:1070–1084PubMedPubMedCentralGoogle Scholar
  25. Harris JC, Hrmova M, Lopato S, Langridge P (2011) Modulation of plant growth by HD-Zip class I and II transcription factors in response to environmental stimuli. New Phytol 190:823–837PubMedCrossRefPubMedCentralGoogle Scholar
  26. Henriksson E, Olsson AS, Johannesson H et al (2005) Homeodomain leucine zipper class I genes in Arabidopsis. Expression patterns and phylogenetic relationships. Plant Physiol 139:509–518PubMedPubMedCentralCrossRefGoogle Scholar
  27. Hu R, Chi X, Chai G et al (2012) Genome-Wide identification, evolutionary expansion, and expression profile of homeodomain-leucine zipper gene family in poplar (Populus trichocarpa). PLoS One 7:e31149PubMedPubMedCentralCrossRefGoogle Scholar
  28. Hu W, Wang L, Tie W et al (2016) Genome-wide analyses of the bZIP family reveal their involvement in the development, ripening and abiotic stress response in banana. Sci Rep 6:30203PubMedPubMedCentralCrossRefGoogle Scholar
  29. Javelle M, Klein-Cosson C, Vernoud V et al (2011) Genome-wide characterization of the HD-ZIP IV transcription factor family in maize: preferential expression in the epidermis. Plant Physiol 157:790–803PubMedPubMedCentralCrossRefGoogle Scholar
  30. Kamata N, Okada H, Komeda Y, Takahashi T (2013) Mutations in epidermis-specific HD-ZIP IV genes affect floral organ identity in Arabidopsis thaliana. Plant J 75:430–440PubMedCrossRefPubMedCentralGoogle Scholar
  31. Kuang JF, Chen L, Shan W et al (2013) Molecular characterization of two banana ethylene signaling component MaEBFs during fruit ripening. Postharvest Biol Technol 85:94–101CrossRefGoogle Scholar
  32. Kuang JF, Chen JY, Liu XC et al (2017) The transcriptional regulatory network mediated by banana (Musa acuminata) dehydration-responsive element binding (MaDREB) transcription factors in fruit ripening. New Phytol 214:762–781PubMedCrossRefPubMedCentralGoogle Scholar
  33. Lehti-Shiu MD, Panchy N, Wang P et al (2017) Diversity, expansion, and evolutionary novelty of plant DNA-binding transcription factor families. Biochim Biophys Acta Gene Regul Mech 1860:3–20PubMedCrossRefPubMedCentralGoogle Scholar
  34. Li C, Zhao M, Ma X et al (2019) The HD-Zip transcription factor LcHB2 regulates litchi fruit abscission through the activation of two cellulase genes. J Exp Bot 70:5189–5203PubMedPubMedCentralCrossRefGoogle Scholar
  35. Lin Z, Hong Y, Yin M et al (2008) A tomato HD-Zip homeobox protein, LeHB-1, plays an important role in floral organogenesis and ripening. Plant J 55:301–310PubMedPubMedCentralCrossRefGoogle Scholar
  36. Liu J, Zhang J, Zhang J et al (2017) Genome-wide analysis of banana MADS-box family closely related to fruit development and ripening. Sci Rep 7:3467PubMedPubMedCentralCrossRefGoogle Scholar
  37. Ma X, Li C, Huang X et al (2019) Involvement of HD-ZIP I transcription factors LcHB2 and LcHB3 in fruitlet abscission by promoting transcription of genes related to the biosynthesis of ethylene and ABA in litchi. Tree Physiol 39:1600–1613PubMedCrossRefPubMedCentralGoogle Scholar
  38. Manavella PA, Dezar CA, Bonaventure G et al (2008) HAHB4, a sunflower HD-Zip protein, integrates signals from the jasmonic acid and ethylene pathways during wounding and biotic stress responses. Plant J 56:376–388PubMedCrossRefGoogle Scholar
  39. Martin G, Baurens FC, Droc G et al (2016) Improvement of the banana “Musa acuminata” reference sequence using NGS data and semi-automated bioinformatics methods. BMC Genom 17:243CrossRefGoogle Scholar
  40. Ohashiito K, Fukuda H (2003) HD-zip III homeobox genes that include a novel member, ZeHB-13 (Zinnia)/ATHB-15 (Arabidopsis), are involved in procambium and xylem cell differentiation. Plant Cell Physiol 44:1350–1358CrossRefGoogle Scholar
  41. Pandey A, Misra P, Alok A et al (2016) Genome-wide identification and expression analysis of homeodomain leucine zipper subfamily IV (HDZ IV) gene family from Musa accuminata. Front Plant Sci 7:20PubMedPubMedCentralGoogle Scholar
  42. Prigge MJ, Otsuga D, Alonso JM et al (2005) Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 17:61–76PubMedPubMedCentralCrossRefGoogle Scholar
  43. Sainsbury F, Thuenemann EC, Lomonossoff GP (2009) pEAQ: versatile expression vectors for easy and quick transient expression of heterologous proteins in plants. Plant Biotechnol J 7:682–693PubMedCrossRefPubMedCentralGoogle Scholar
  44. Schena M, Lloyd AM, Davis RW (1993) The HAT4 gene of Arabidopsis encodes a developmental regulator. Genes Dev 7:367–379PubMedCrossRefPubMedCentralGoogle Scholar
  45. Sessa G, Steindler C, Morelli G, Ruberti I (1998) The Arabidopsis Athb-8, -9 and genes are members of a small gene family coding for highly related HD-ZIP proteins. Plant Mol Biol 38:609–622PubMedCrossRefPubMedCentralGoogle Scholar
  46. Shao J, Haider I, Xiong L et al (2018) Functional analysis of the HD-Zip transcription factor genes Oshox12 and Oshox14 in rice. PLoS One 13:e0199248PubMedPubMedCentralCrossRefGoogle Scholar
  47. Stamm P, Kumar PP (2010) The phytohormone signal network regulating elongation growth during shade avoidance. J Exp Bot 61:2889–2903PubMedCrossRefPubMedCentralGoogle Scholar
  48. Tan XL, Fan ZQ, Shan W et al (2018) Association of BrERF72 with methyl jasmonate-induced leaf senescence of Chinese flowering cabbage through activating JA biosynthesis-related genes. Hortic Res 5:22PubMedPubMedCentralCrossRefGoogle Scholar
  49. Tan XL, Fan ZQ, Kuang JF et al (2019) Melatonin delays leaf senescence of Chinese flowering cabbage by suppressing ABFs-mediated abscisic acid biosynthesis and chlorophyll degradation. J Pineal Res 67:e12570PubMedCrossRefPubMedCentralGoogle Scholar
  50. Turchi L, Carabelli M, Ruzza V et al (2013) Arabidopsis HD-Zip II transcription factors control apical embryo development and meristem function. Development 140:2118–2129PubMedCrossRefPubMedCentralGoogle Scholar
  51. Turchi L, Baima S, Morelli G, Ruberti I (2015) Interplay of HD-Zip II and III transcription factors in auxin-regulated plant development. J Exp Bot 66:5043–5053PubMedCrossRefPubMedCentralGoogle Scholar
  52. Wan CY, Wilkins TA (1994) A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.). Anal Biochem 223:7–12PubMedCrossRefPubMedCentralGoogle Scholar
  53. Xiao YY, Kuang JF, Qi XN et al (2018) A comprehensive investigation of starch degradation process and identification of a transcriptional activator MabHLH6 during banana fruit ripening. Plant Biotechnol J 16:151–164PubMedCrossRefPubMedCentralGoogle Scholar
  54. Yan T, Li L, Xie L et al (2018) A novel HD-ZIP IV/MIXTA complex promotes glandular trichome initiation and cuticle development in Artemisia annua. New Phytol 218:567–578PubMedCrossRefPubMedCentralGoogle Scholar
  55. Yang Q, Niu Q, Li J et al (2018) PpHB22, a member of HD-Zip proteins, activates PpDAM1 to regulate bud dormancy transition in ‘Suli’ pear (Pyrus pyrifolia White Pear Group). Plant physiol Bioch 127:355–365CrossRefGoogle Scholar
  56. Zhang L, Zhou D, Hu H et al (2019) Genome-wide characterization of a SRO gene family involved in response to biotic and abiotic stresses in banana (Musa spp.). BMC Plant Biol 19:211PubMedPubMedCentralCrossRefGoogle Scholar
  57. Zhu H, Sun X, Zhang Q et al (2018) GLABROUS (CmGL) encodes a HD-ZIP IV transcription factor playing roles in multicellular trichome initiation in melon. Theor Appl Genet 131:569–579PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources/Guangdong Provincial Key Laboratory of Postharvest, Science of Fruits and Vegetables/Engineering Research Center of Southern Horticultural Products Preservation, Ministry of Education, College of HorticultureSouth China Agricultural UniversityGuangzhouChina

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