Physiology and Molecular Biology of Plants

, Volume 25, Issue 1, pp 263–275 | Cite as

Profiling of indole metabolic pathway in thermo-sensitive Bainong male sterile line in wheat (Triticum aestivum L.)

  • Qing Su
  • Jing Yang
  • Qing Yun Fu
  • Fei Yun Jia
  • Suo Ping Li
  • Yong Li
  • You Yong LiEmail author
Research Article


Bainong male sterile (BNS) wheat (Triticum aestivum L.) is a thermo-sensitive genic male sterile line with excellent sterility and self-restoration. We focused on transcriptional profiles of differentially expressed probes between BNS sterile and fertile anthers. Anthers, rachis and spikes from sterile line and fertile line were collected. Extracted RNA was assayed using wheat expression microarray and Gene Ontology was analyzed using Cytoscape with ClueGO. An indole (indole-3-acetic acid: IAA) metabolism pathway sub-network was almost formed in all differentially expressed profiles between sterile and fertile samples. IAA sub-network contained four nodes of indole and alkaloid metabolism connecting main network via indole compounds. This sub-network was absent in rachis and intact in transformed fertile anthers, which was the main differently expressed metabolism pathway in F1 anthers with restorer genes. Alkaloid metabolism was absent in sterile anthers. Abnormal metabolism of IAA may be involved in BNS sterility. BNS transformation may be regulated by the production of IAA and alkaloid metabolism pathway, which favor the safe utilization of the sterile line in hybrid wheat production.


Alkaloid metabolism BNS male sterility Gene expression microarray IAA metabolism Wheat 



This research was funded by Henan Research Project on Foundation and Frontier Technology (Nos. 122300410011 and 162300410136). We would like to thank prof. ZhenGang Ru, Directorate of Wheat Research Center in Henan institute of science and technology, for supply wheat BNS sterile line. We would also like to thank prof. Gonmbia who give many suggestions for ClueGO running.

Compliance with ethical standards

Conflict of interest

The authors have no conflict of interest to declare.

Supplementary material

12298_2018_626_MOESM1_ESM.doc (40 kb)
Supplementary material 1 (DOC 39 kb)


  1. Al-Whaibi MH (2011) Plant heat shock proteins: a mini review. J King Saud Univ 23:139–150CrossRefGoogle Scholar
  2. Bindea G et al (2009) ClueGO: a Cytoscape plug-into decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics 25:1091–1093. CrossRefGoogle Scholar
  3. Crismani W et al (2006) Microarray expression analysis of meiosis and microsporogenesis in hexaploid bread wheat. BMC Genom 7:267. CrossRefGoogle Scholar
  4. Daraselia N, Yuryev A, Egorov S, Mazo I, Ispolatov I (2007) Automatic extraction of gene ontology annotation and its correlation with clusters in protein networks. BMC Bioinform 8:243. CrossRefGoogle Scholar
  5. Du LJ, Sun HY, Su Q, A-l BA, Li YY (2016) Average temperature above 15°C significantly affect fertility transition of thermo-sensitive Male Sterile Wheat BNS. Chin J Agrometeorol 37:555–563Google Scholar
  6. Fan XJ et al (2015) Hereditary stability and restoration of thermo-photo-sensitive male sterile line BNS of wheat (Triticum aestivum L.). J Northwest A&F Univ (NatSciEd) 43:53–58Google Scholar
  7. Fei H, Zhang R, Pharis RP, Sawhney VK (2004) Pleiotropic effects of the male sterile33 (ms33) mutation in Arabidopsis are associated with modifications in endogenous gibberellins, indole-3-acetic acid and abscisic acid. Planta 219:649–660. CrossRefGoogle Scholar
  8. Feki K, Kamoun Y, Ben Mahmoud R, Farhat-Khemakhem A, Gargouri A, Brini F (2015) Multiple abiotic stress tolerance of the transformants yeast cells and the transgenic Arabidopsis plants expressing a novel durum wheat catalase. Plant Physiol Biochem 97:420–431. CrossRefGoogle Scholar
  9. He ZC, Xiao YH (1992) Effect of the regulators on fertility in HPGMR (58S). Hybrid Rice 7(3):39–42Google Scholar
  10. Hu J, Chen G, Zhang H, Qian Q, Ding Y (2016) Comparative transcript profiling of alloplasmic male-sterile lines revealed altered gene expression related to pollen development in rice (Oryza sativa L.). BMC Plant Biol 16:175. CrossRefGoogle Scholar
  11. Kovaleva LV, Voronkov AS, Zakharova EV, Andreev IM (2018) ABA and IAA control microsporogenesis in Petunia hybrida L. Protoplasma 255:751–759. CrossRefGoogle Scholar
  12. Li NH, Tong Z, Lu SF (2000) Immunohistochemical analysis of IAA in anthers of the photoperiod-sensitive genic male-sterile rice. Acta Botanica Sinica 42:1045–1050Google Scholar
  13. Li YF, Zhao CP, Zhang FT, Sun H, Sun DF (2006) Fertility alteration in the photo-thermo-sensitive male sterile line BS20 of wheat (Triticum aestivum L.). Euphytica 151:207–213CrossRefGoogle Scholar
  14. Li LJ, Ru ZG, Gao QR, Jiang H, Guo FZ, Wu SW, Sun Z (2009) Male sterility and thermo-photo sensitivity characterisitics of BNS in wheat. Sci Agric Sin 42:3019–3027Google Scholar
  15. Li SX, Gu J, Tian YX, Liu K, Yang HX, Zhao H, Yang MJ (2011a) Advance of hybrid wheat seed production in Yunnan. Seed 30:59–62Google Scholar
  16. Li YY, Ru ZG, Su Q, Fu QY (2011b) Identification and analysis of differentially expressed proteins of BNS male sterile line and its conversion line of wheat. Acta Agron Sin 37:1540–1550CrossRefGoogle Scholar
  17. Li YY, Li Y, Fu QY, Sun HH, Ru ZG (2015) Anther proteomic characterization in temperature sensitive Bainong male sterile wheat. Biol Plant 59:273–282CrossRefGoogle Scholar
  18. Ma XF, Wang Z, Li XY, Liu F, Fan XJ, Ma LJ (2013) Restoring ability test and heterosis analysis of wheat thermo-photo-sensitive genic male sterile line BNS. Acta Agric Boteali-occidentalis Sin 22:90–94Google Scholar
  19. Meng C et al (2017) Transcriptome profiling reveals the genetic basis of alkalinity tolerance in wheat. BMC Genom 18:24. CrossRefGoogle Scholar
  20. Murai K, Tsutui I, Kawanishi Y, Ikeguchi S, Yanaka M, Ishikawa N (2008) Development of photoperiod-sensitive cytoplasmic male sterile (PCMS) wheat lines showing high male sterility under long-day conditions and high seed fertility under short-day conditions. Euphytica 159:315–323CrossRefGoogle Scholar
  21. Ning JQ, Ru ZG, Zheng WJ, Chai SC (2011) Male sterility and restoration of thermo-photo-sensitive male sterile line BNS of common wheat (Triticum aestivum L.). Journal of Triticeae Crops 31:642–647Google Scholar
  22. Oshino T, Abiko M, Saito R, Ichiishi E, Endo M, Kawagishi-Kobayashi M, Higashitani A (2007) Premature progression of anther early developmental programs accompanied by comprehensive alterations in transcription during high-temperature injury in barley plants. Mol Genet Genomics 278:31–42. CrossRefGoogle Scholar
  23. Pan Y et al (2014) Genes associated with thermosensitive genic male sterility in rice identified by comparative expression profiling. BMC Genom 15:1114. CrossRefGoogle Scholar
  24. Qin Z, Sun HY, Fu QY, Wei X, Ba A, Ru ZG, Li YY (2018) Study on significant effects of temperature changes in winter and spring on fertility conversion of wheat thermo-sensitive male sterile line BNS. Acta Agric Boreali-occidentalis Sin 27:31–37Google Scholar
  25. Shannon P et al (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504. CrossRefGoogle Scholar
  26. Simmonds J et al (2004) Oxalate oxidase: a novel reporter gene for monocot and dicot transformations. Mol Breeding 13:79–91CrossRefGoogle Scholar
  27. Singh SP, Srivastava R, Kumar J (2015) Male sterility systems in wheat and opportunities for hybrid wheat development. Acta Physiol Plant 37:1713CrossRefGoogle Scholar
  28. Su SQ, Ru ZG, Qin ZY, Cao YP, Liu FF, Li YY (2013) Differential expression of small heat shock protein gene (hsp23.5) between wheat (Triticum aestivum L.) BNS male sterile line and its conversion line. J Agric Biotechnol 21:29–37Google Scholar
  29. Sun HH, Yang J, Wei X, Fu QY, Cao YP, Ru ZG, Li YY (2016) Detection of linkage groups and location of QTLs in Chinese Spring for restoring wheat BNS male sterility. J Tritceae Crops 36:856–865Google Scholar
  30. Suzuki H, Rodriguez-Uribe L, Xu J, Zhang J (2013) Transcriptome analysis of cytoplasmic male sterility and restoration in CMS-D8 cotton. Plant Cell Rep 32:1531–1542. CrossRefGoogle Scholar
  31. Tang RS, Mei CS, Zhang JY, Cai XN, Wu GN (1996) Relationship between rice male sterility induction by TO3 and level of endogenous hormones. Jiangsu J Agric Sci 12:6–10Google Scholar
  32. Tang JH, He ZY, Chen WC, Tan YS, Xie HL, Li DL (2003) Relationship between fertility conversion and endogenous hormones in a maize thermo-sensitive genic male-sterile line. Acta Agron Sin 29:336–338Google Scholar
  33. Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971. CrossRefGoogle Scholar
  34. Zhang JK, Feng L, Luo D, Yu GD, Shi YM, Li BQ (2001) Effect on the fertility of thermo-photo-sensitive genic male-sterile wheat C49S using different chemicals. J Triticeae Crops 21:69–72Google Scholar
  35. Zhang JK, Zong XF, Yu GD, Li JN, Zhang W (2006) Relationship between phytohormones and male sterility in thermo-photo-sensitive genic male sterile (TGMS) wheat. Euphytica 150:241–248CrossRefGoogle Scholar
  36. Zhang BL et al (2013a) Genetic analysis on male sterility of thermo-photo-sensitive male sterile line BNS in wheat. Sci Agric Sin 46:1533–1542Google Scholar
  37. Zhang YY et al (2013b) Dynamic changes of endogenous hormones in thermo-photo-sensitive male sterile wheat line BNS. Acta Bot Boreali-Occidentalia Sin 33:1165–1170Google Scholar
  38. Zhang ZG et al (2016) Relationship between fertility transition of thermo-photo-sensitive wheat male sterile line BNS and endogenous hormone contents in its developing ear. J Plant Genet Resour 17:913–919Google Scholar
  39. Zhao CP (2010) Status and trends of hybrid wheat research in China. J Agric Sci Technol 12:5–8Google Scholar
  40. Zhao YJ, Tong Z, Chen HJ, Jin YJ (1996) Relationship between male fertility and endogenous phytohormones in photoperiod - sensitive genic male sterile rice. Acta Bot Sin 38:936–941Google Scholar
  41. Zhao DH, Sun HH, Yu TY, Li YY (2014) Gene atp1 expresses differentially between BNS male sterile line and its conversion line in wheat. Life Sci Res 18:488–493Google Scholar
  42. Zhou M, Ru Z, Luo Y, Luo P, Li Q, Guo X, Zhou P (2010) Male fertility transformation of two-line wheat sterile lines BNS. J Nuclear Agric Sci 24:887–894Google Scholar
  43. Zhou X, Liu Z, Ji R, Feng H (2017) Comparative transcript profiling of fertile and sterile flower buds from multiple-allele-inherited male sterility in Chinese cabbage (Brassica campestris L. ssp. pekinensis). Mol Genet Genomics 292:967–990. CrossRefGoogle Scholar

Copyright information

© Prof. H.S. Srivastava Foundation for Science and Society 2018

Authors and Affiliations

  • Qing Su
    • 1
    • 2
  • Jing Yang
    • 1
  • Qing Yun Fu
    • 1
  • Fei Yun Jia
    • 1
  • Suo Ping Li
    • 2
  • Yong Li
    • 1
    • 3
  • You Yong Li
    • 1
    Email author
  1. 1.Henan Institute of Science and Technology/Collaborative Innovation Center of Modern Biological BreedingXinxiangChina
  2. 2.Henan UniversityKaifengChina
  3. 3.Institute of Plant Physiology and EcologySIBS, CASShanghaiChina

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