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Theoretical and Applied Genetics

, Volume 130, Issue 8, pp 1693–1703 | Cite as

A mutant in the CsDET2 gene leads to a systemic brassinosteriod deficiency and super compact phenotype in cucumber (Cucumis sativus L.)

  • Shanshan Hou
  • Huanhuan Niu
  • Qianyi Tao
  • Shenhao Wang
  • Zhenhui Gong
  • Sen Li
  • Yiqun WengEmail author
  • Zheng LiEmail author
Original Article

Abstract

Key message

A novel dwarf cucumber mutant, scp-2, displays a typical BR biosynthesis-deficient phenotype, which is due to a mutation in CsDET2 for a steroid 5-alpha-reductase.

Abstract

Brassinosteroids (BRs) are a group of plant hormones that play important roles in the development of plant architecture, and extreme dwarfism is a typical outcome of BR-deficiency. Most cucumber (Cucumis sativus L.) varieties have an indeterminate growth habit, and dwarfism may have its value in manipulation of plant architecture and improve production in certain production systems. In this study, we identified a spontaneous dwarf mutant, super compact-2 (scp-2), that also has dark green, wrinkle leaves. Genetic analyses indicated that scp-2 was different from two previously reported dwarf mutants: compact (cp) and super compact-1 (scp-1). Map-based cloning revealed that the mutant phenotype was due to two single nucleotide polymorphism and a single-base insertion in the CsDET2 gene that resulted in a missense mutation in a conserved amino acid and thus a truncated protein lacking the conserved catalytic domains in the predicted steroid 5α-reductase protein. Measurement of endogenous hormone levels indicated a reduced level of brassinolide (BL, a bioactive BR) in scp-2, and the mutant phenotype could be partially rescued by the application of epibrassinolide (EBR). In addition, scp-2 mutant seedlings exhibited dark-grown de-etiolation, and defects in cell elongation and vascular development. These data support that scp-2 is a BR biosynthesis-deficient mutant, and that the CsDET2 gene plays a key role in BR biosynthesis in cucumber. We also described the systemic BR responses and discussed the specific BR-related phenotypes in cucumber plants.

Keywords

Gibberellic Acid Male Flower Dwarf Mutant Cucumber Chromosome Wrinkled Leaf 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

The authors thank Kristin Haider (USDA-ARS) for technical help and Professor Xiaofeng Wang (Northwest A&F University) for valuable suggestions on BR-related analysis. ZL and SL’s work in the University of Wisconsin at Madison visit was partially supported by the China Scholarship Council. This work was supported by the National Natural Science Foundation of China (Nos. 31471879, 31672150) (to ZL), the Innovation of Agricultural Science and Technology in Shaanxi Province (No. 2015NY081) (to ZL), the Young Talent Cultivation Project (Northwest A&F University) (to ZL) and the Agriculture and Food Research Initiative Competitive Grant 2013-67013-21105 from the U.S. Department of Agriculture National Institute of Food (to YW).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

122_2017_2919_MOESM1_ESM.pdf (899 kb)
Supplementary material 1 (PDF 898 kb)

References

  1. Alabadí D, Gil J, Blázquez MA, García-Martínez JL (2004) Gibberellins repress photomorphogenesis in darkness. Plant Physiol 134:1050–1057CrossRefPubMedPubMedCentralGoogle Scholar
  2. An Y, Zhou H, Zhong M, Sun J, Shu S, Shao Q, Guo S (2016) Root proteomics reveals cucumber 24-epibrassinolide responses under Ca(NO3)2 stress. Plant Cell Rep 35:1081–1101CrossRefPubMedGoogle Scholar
  3. Atsmon D (1968) The interaction of genetic, environmental, and hormonal factors in stem elongation and floral development of cucumber plants. Ann Bot 32:877–882CrossRefGoogle Scholar
  4. Bai M, Shang J, Oh E, Fan M, Bai Y, Zentella R, Sun T, Wang Z (2012) Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat Cell Biol 14:810–817CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bajguz A (2011) Brassinosteroids: a class of plant hormone: brassinosteroids—occurrence and chemical structures in plants. Wiley-Interscience, New York, pp 1–27CrossRefGoogle Scholar
  6. Bishop GJ (2003) Brassinosteroid mutants of crops. J Plant Growth Regul 22:325–335CrossRefPubMedGoogle Scholar
  7. Bishop GJ, Harrison K, Jones JDG (1996) The tomato Dwarf gene isolated by heterologous transposon tagging encodes the first member of a new cytochrome P450 family. Plant Cell 8:959–969CrossRefPubMedPubMedCentralGoogle Scholar
  8. Cavagnaro PF, Senalik DA, Yang L, Simon PW, Harkins TT, Kodira CD, Huang S, Weng Y (2010) Genome-wide characterization of simple sequence repeats in cucumber (Cucumis sativus L.). BMC Genom 11:569CrossRefGoogle Scholar
  9. Chory J, Nagpal P, Peto CA (1991) Phenotypic and genetic analysis of det2, a new mutant that affects light-regulated seedling development in Arabidopsis. Plant Cell 3:445–459CrossRefPubMedPubMedCentralGoogle Scholar
  10. Clouse SD, Sasse JM (1998) Brassinosteroids: essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol 49:427–451CrossRefPubMedGoogle Scholar
  11. Clouse SD, Langford M, McMorris TC (1996) A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol 111:671–678CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cramer CS, Wehner TC (2000) Path analysis of the correlation between fruit number and plant traits of cucumber populations. HortScience 35:708–711Google Scholar
  13. Crienen J, Reuling G, Segers B, van de Wal M (2009) New cucumber plants with a compact growth habit. Patent, International publication number WO 2009/059777 A1Google Scholar
  14. Fazio G, Staub JE, Stevens MR (2003) Genetic mapping and QTL analysis of horticultural traits in cucumber (Cucumis sativus L.) using recombinant inbred lines. Theor Appl Genet 107:864–874CrossRefPubMedGoogle Scholar
  15. Fu F, Mao W, Shi K, Zhou Y, Asami T, Yu J (2008) A role of brassinosteroids in early fruit development in cucumber. J Exp Bot 59:2299–2308CrossRefPubMedPubMedCentralGoogle Scholar
  16. Fujioka S, Li J, Choi YH, Seto H, Takatsuto S, Watanabe T, Kuriyama H, Yokota T et al (1997) The Arabidopsis de-etiolated2 mutant is blocked early in brassinosteroid biosynthesis. Plant Cell 9:1951–1962CrossRefPubMedPubMedCentralGoogle Scholar
  17. Grove MD, Spencer GF, Rohwedder WK, Mandava NB, Worley JF, Warthen JD, Steffens GL, Flippen-Anderson JL et al (1979) Brassinolide, a plant growth-promoting steroid isolated from Brassica napus pollen. Nature 281:216–217CrossRefGoogle Scholar
  18. Gudesblat GE, Russinova E (2011) Plants grow on brassinosteroids. Curr Opin Plant Biol 14:530–537CrossRefPubMedGoogle Scholar
  19. Hartwig T, Chuck GS, Fujioka S, Klempien A, Weizbauer R, Potluri DP, Choe S, Johal GS et al (2011) Brassinosteroid control of sex determination in maize. Proc Natl Acad Sci USA 108:19814–19819CrossRefPubMedPubMedCentralGoogle Scholar
  20. Hedden P (2003) The genes of the green revolution. Trends Genet 19:5–9CrossRefPubMedGoogle Scholar
  21. Kauffman CS, Lower RL (1976) Inheritance of an extreme dwarf plant type in the cucumber. J Am Sci Hortic Sci 101:150–151Google Scholar
  22. Kojima M, Kamada-Nobusada T, Komatsu H, Takei K, Kuroha T, Mizutani M, Ashikari M, Ueguchi- Tanaka M et al (2009) Highly sensitive and high-throughput analysis of plant hormones using MS-probe modification and liquid chromatography-tandem mass spectrometry: an application for hormone profiling in Oryza sativa. Plant Cell Physiol 50:1201–1214CrossRefPubMedPubMedCentralGoogle Scholar
  23. Kubicki B, Soltysiak U, Korzeniewska A (1986) Induced mutations in cucumber (Cucumis sativus L.) V. Compact type of growth. Genet Pol 27:289–298Google Scholar
  24. Levinson G, Gutman GA (1987) Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol Bio Evol 4:203–221Google Scholar
  25. Li J, Nagpal P, Vitart V, McMorris TC, Chory J (1996) A role for brassinosteroids in light-dependent development of Arabidopsis. Science 272:398–401CrossRefPubMedGoogle Scholar
  26. Li Z, Pan J, Guan Y, Tao Q, He H, Si L, Cai R (2008) Development and fine mapping of three co-dominant SCAR markers linked to the M/m gene in the cucumber plant (Cucumis sativus L.). Theor Appl Genet 117:1253–1260CrossRefPubMedGoogle Scholar
  27. Li Y, Yang L, Pathak M, Li D, He X, Weng Y (2011) Fine genetic mapping of cp: a recessive gene for compact (dwarf) plant architecture in cucumber, Cucumis sativus L. Theor Appl Genet 123:973–983CrossRefPubMedGoogle Scholar
  28. Li Z, Wang S, Tao Q, Pan J, Si L, Gong Z, Cai R (2012) A putative positive feedback regulation mechanism in CsACS2 expression suggests a modified model for sex determination in cucumber (Cucumis sativus L.). J Exp Bot 63:4475–4484CrossRefPubMedPubMedCentralGoogle Scholar
  29. Li P, Chen L, Zhou Y, Xia X, Shi K, Chen Z, Yu J (2013) Brassinosteroids-induced systemic stress tolerance was associated with increased transcripts of several defence-related genes in the phloem in Cucumis sativus. PLoS One 8:e66582CrossRefPubMedPubMedCentralGoogle Scholar
  30. Lin T, Wang S, Zhong Y, Gao D, Cui Q, Chen H, Zhang Z, Shen H et al (2016) A truncated F-box protein confers the dwarfism in cucumber. J Genet Genom 43:223–226CrossRefGoogle Scholar
  31. Michelmore RW, Paran I, Kesseli RV (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci USA 88:9828–9832CrossRefPubMedPubMedCentralGoogle Scholar
  32. Niemirowicz-Szczytt K, Rucinska M, Korzeniewsia A (1996) An induced mutation in cucumber (Cucumis sativus L.): super compact. Cucurbit Genet Coop Rep 19:1–3 (article 1) Google Scholar
  33. Noguchi T, Fujioka S, Takatsuto S, Sakurai A, Yoshida S, Li J, Chory J (1999) Arabidopsis det2 is defective in the conversion of (24R)-24-methylcholest-4-en-3-one to (24R)-24-methy-5α-cholestan-3-one in brassinosteroid biosynthesis. Plant Physiol 120:833–839CrossRefPubMedPubMedCentralGoogle Scholar
  34. Nomura T, Jager CE, Kitasaka Y, Takeuchi K, Fukami M, Yoneyama K, Matsushita Y, Nyunoya H et al (2004) Brassinosteroid deficiency due to truncated steroid 5α-reductase causes dwarfism in the lk mutant of pea. Plant Physiol 135:2220–2229CrossRefPubMedPubMedCentralGoogle Scholar
  35. Peng J, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE, Beales J, Fish LJ et al (1999) ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400:256–261CrossRefPubMedGoogle Scholar
  36. Russell DE, Wilson JD (1994) Steroid 5 α-reductase: two genes/two enzymes. Annu Rev Biochem 63:25–61CrossRefPubMedGoogle Scholar
  37. Shimada Y, Goda H, Nakamura A, Takatsuto S, Fujioka S, Yoshida S (2003) Organ-specific expression of brassinosteroid-biosynthetic gene and distribution of endogenous brassinosteroids in Arabidopsis. Plant Physiol 131:287–297CrossRefPubMedPubMedCentralGoogle Scholar
  38. Steber CM, McCourt P (2001) A role for brassinosteroids in germination in Arabidopsis. Plant Physiol 125:763–769CrossRefPubMedPubMedCentralGoogle Scholar
  39. Suzuki Y, Saso K, Fujioka S, Yoshida S, Nitasaka E, Nagata S, Nagasawa H, Takatsuto S et al (2003) A dwarf mutant strain of Pharbitis nil, Uzukobito (kobito), has defective brassinosteroid biosynthesis. Plant J 36:401–410CrossRefPubMedGoogle Scholar
  40. Symons GM, Reid JB (2004) Brassinosteroids do not undergo long-distance transport in pea. Implications for the regulation of endogenous brassinosteroid levels. Plant Physiol 135:2196–2206CrossRefPubMedPubMedCentralGoogle Scholar
  41. Symons GM, Schultz L, Kerckhoffs LH, Davies NW, Gregory D, Reid JB (2002) Uncoupling brassinosteroid levels and de-etiolation in pea. Physiol Plant 115:311–319CrossRefPubMedGoogle Scholar
  42. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefPubMedPubMedCentralGoogle Scholar
  43. Tan J, Tao Q, Niu H, Zhang Z, Li D, Gong Z, Weng Y, Li Z (2015) A novel allele of monoecious (m) locus is responsible for elongated fruit shape and perfect flowers in cucumber (Cucumis sativus L.). Theor Appl Genet 128:2483–2493CrossRefPubMedGoogle Scholar
  44. Wang L, Wang Z, Xu Y, Joo SH, Lim SK, Xue Z, Xu Z, Wang Z et al (2009) OsGSR1 is involved in crosstalk between gibberellins and brassinosteroids in rice. Plant J 57:498–510CrossRefPubMedGoogle Scholar
  45. Wang B, Li Y, Zhang W (2012) Brassinosteroids are involved in response of cucumber (Cucumis sativus) to iron deficiency. Ann Bot 110:681–688CrossRefPubMedPubMedCentralGoogle Scholar
  46. Wang H, Li W, Qin Y, Pan Y, Wang X, Weng Y, Chen P, Li Y (2017) The cytochrome P450 gene CsCYP85A1 is a putative candidate for super compact-1 (scp-1) plant architecture mutation in cucumber (Cucumis sativus L.). Front Plant Sci 8:266PubMedPubMedCentralGoogle Scholar
  47. Wei L, Deng X, Zhu T, Zheng T, Li P, Wu J, Zhang D, Lin H (2015) Ethylene involved in brassinosteroids induced alternative respiratory pathway in cucumber (Cucumis sativus L.) seedlings response to abiotic stress. Front Plant Sci 6:982PubMedPubMedCentralGoogle Scholar
  48. Wu Q, Wu D, Shen Z, Duan C, Guan Y (2013) Quantification of endogenous brassinosteroids in plant by on-line two-dimensional microscale solid phase extraction-on column derivatization coupled with high performance liquid chromatography-tandem mass spectrometry. J Chromatogr A 1297:56–63CrossRefPubMedGoogle Scholar
  49. Xia X, Zhou Y, Ding J, Shi K, Asami T, Chen Z, Yu J (2011) Induction of systemic stress tolerance by brassinosteroid in Cucumis sativus. New Phytol 191:706–720CrossRefPubMedGoogle Scholar
  50. Yang L, Koo D-H, Li Y, Zhang X, Luan F, Havey MJ, Jiang J, Weng Y (2012) Chromosome rearrangements during domestication of cucumber as revealed by high-density genetic mapping and draft genome assembly. Plant J 71:895–906CrossRefPubMedGoogle Scholar
  51. Ye Q, Zhu W, Li L, Zhang S, Yin Y, Ma H, Wang X (2010) Brassinosteroids control male fertility by regulating the expression of key genes involved in Arabidopsis anther and pollen development. Proc Natl Acad Sci USA 107:6100–6105CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.College of HorticultureNorthwest A&F UniversityYanglingChina
  2. 2.Horticulture DepartmentUniversity of WisconsinMadisonUSA
  3. 3.Horticulture CollegeShanxi Agricultural UniversityTaiguChina
  4. 4.USDA ARS, Vegetable Crops Research UnitMadisonUSA

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