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Plant Molecular Biology

, Volume 97, Issue 1–2, pp 131–147 | Cite as

A novel mitochondrial orf147 causes cytoplasmic male sterility in pigeonpea by modulating aberrant anther dehiscence

  • Pooja Bhatnagar-Mathur
  • Ranadheer Gupta
  • Palakolanu Sudhakar Reddy
  • Bommineni Pradeep Reddy
  • Dumbala Srinivas Reddy
  • C. V. Sameerkumar
  • Rachit Kumar Saxena
  • Kiran K. Sharma
Article
  • 305 Downloads

Abstract

Key message

A novel open reading frame (ORF) identified and cloned from the A4 cytoplasm of Cajanus cajanifolius induced partial to complete male sterility when introduced into Arabidopsis and tobacco.

Abstract

Pigeonpea (Cajanus cajan L. Millsp.) is the only legume known to have commercial hybrid seed technology based on cytoplasmic male sterility (CMS). We identified a novel ORF (orf147) from the A4 cytoplasm of C. cajanifolius that was created via rearrangements in the CMS line and co-transcribes with the known and unknown sequences. The bi/poly-cistronic transcripts cause gain-of-function variants in the mitochondrial genome of CMS pigeonpea lines having distinct processing mechanisms and transcription start sites. In presence of orf147, significant repression of Escherichia coli growth indicated its toxicity to the host cells and induced partial to complete male sterility in transgenic progenies of Arabidopsis thaliana and Nicotiana tabacum where phenotype co-segregated with the transgene. The male sterile plants showed aberrant floral development and reduced lignin content in the anthers. Gene expression studies in male sterile pigeonpea, Arabidopsis and tobacco plants confirmed down-regulation of several anther biogenesis genes and key genes involved in monolignol biosynthesis, indicative of regulation of retrograde signaling. Besides providing evidence for the involvement of orf147 in pigeonpea CMS, this study provides valuable insights into its function. Cytotoxicity and aberrant programmed cell death induced by orf147 could be important for mechanism underlying male sterility that offers opportunities for possible translation for these findings for exploiting hybrid vigor in other recalcitrant crops as well.

Keywords

Arabidopsis Cajanus cajan Cytoplasmic male sterility Hybrid vigor Pigeonpea Tobacco 

Notes

Acknowledgements

This work was undertaken as part of the CGIAR Research Program on Grain Legumes. Thanks to Rahul Nitnavare, Chavvi Srivastava, Divya and Kedarinath for their technical assistance with the transformation and gene expression studies and PS Rao for photography. Critical reviews of the manuscript by Drs. Gopalan Selvaraj, Rajeev Gupta and Damaris Odeny are gratefully acknowledged.

Author contributions

PBM and KKS conceptualized, designed and analyzed all experimental data. RG conducted expression studies in prokaryotic system, Sequence analysis was done by PSR, BPR assisted in cloning and transformation; DSR was involved in qPCR and Northern blot studies. RKS provided inputs on mitochondrial genomic sequence information and analysis. CVSK provided pigeonpea seed material. PBM and KKS conducted histochemical studies. PBM, KKS, RG and PSR contributed to manuscript preparation.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest. PBM, RG and KKS are inventors on the patent applications of this work and are current employees of ICRISAT who owns the IP.

Supplementary material

11103_2018_728_MOESM1_ESM.doc (102 kb)
Supplementary material 1 (DOC 102 KB)

References

  1. Araya A, Domec C, Begu D, Litvak S (1992) An in vitro system for the editing of ATP synthase subunit 9 mRNA using wheat mitochondrial extracts. Proc Natl Acad Sci USA 89:1040–1044CrossRefPubMedPubMedCentralGoogle Scholar
  2. Balk J, Leaver CJ (2001) The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release. Plant Cell 13:1803–1818CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bergman P, Edqvist J, Farbos I, Glimelius K (2000) Male-sterile tobacco displays abnormal mitochondrial atp1 transcript accumulation and reduced floral ATP/ADP ratio. Plant Mol Biol 42:531–544CrossRefPubMedGoogle Scholar
  4. Bonhomme S, Budar F, Lancelin D, Small I, Defrance M, Pelletier G (1992) Sequence and transcript analysis of the Nco2.5 Ogura-specific fragment correlated with cytoplasmic male sterility in Brassica cybrids. Mol Gen Genet 235:340–348CrossRefPubMedGoogle Scholar
  5. Bonner L, Dickinson H (1989) Anther dehiscence in Lycopersicon esculentum Mill. New Phytol 113:97–115CrossRefGoogle Scholar
  6. Chen L, Liu Y-G (2014) Male sterility and fertility restoration in crops. Annu Rev Plant Biol 65:579–606CrossRefPubMedGoogle Scholar
  7. Clough SJ, Bent AF (1998) Floral dip, a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefPubMedGoogle Scholar
  8. Curtis M, Grossniklaus U (2003) A Gateway TM cloning vector set for high-throughput functional analysis of genes in plants. Plant Physiol 133:462–469CrossRefPubMedPubMedCentralGoogle Scholar
  9. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139:5–17CrossRefPubMedPubMedCentralGoogle Scholar
  10. Dalvi VA, Saxena KB, Madrap IA (2008) Fertility restoration in cytoplasmic-nuclear male-sterile lines derived from 3 wild relatives of pigeonpea. J Hered 99:671–673CrossRefPubMedGoogle Scholar
  11. Dawson J, SÖzen E, Vizir I, Van Waeyenberge S, Wilson ZA, Mulligan BJ (1999) Characterization and genetic mapping of a mutation (ms35) which prevents anther dehiscence in Arabidopsis thaliana by affecting secondary wall thickening in the endothecium. New Phytol 144:213–222CrossRefGoogle Scholar
  12. Dewey RE, Levings CS III, Timothy DH (1986) Novel recombinations in the maize mitochondrial genome produce a unique transcriptional unit in the Texas male-sterile cytoplasm. Cell 44:439–449CrossRefPubMedGoogle Scholar
  13. Dieterich JH, Braun HP, Schmitz UK (2003) Alloplasmic male sterility in Brassica napus (CMS “Tournefortii-Stiewe”) is associated with a special gene arrangement around a novel atp9 gene. Mol Genet Genomics 269:723–731CrossRefPubMedGoogle Scholar
  14. Ding Y, Chan CY, Lawrence CE (2004) Sfold web server for statistical folding and rational design of nucleic acids. Nucleic Acids Res 32(Issue supplement 2):W135–W141CrossRefPubMedPubMedCentralGoogle Scholar
  15. Duroc Y, Gaillard C, Hiard S, Defrance M, Pelletier G, Budar F (2005) Biochemical and functional characterization of ORF138, a mitochondrial protein responsible for Ogura cytoplasmic male sterility in Brassiceae. Biochimie 87:1089–1100CrossRefPubMedGoogle Scholar
  16. Fujii S, Toriyama K (2008) DCW11, Down-regulated gene 11 in CW-type cytoplasmic male sterile rice, encoding mitochondrial protein phosphatase 2C is related to cytoplasmic male sterility. Plant Cell Physiol 49:633–640CrossRefPubMedGoogle Scholar
  17. Fujii S, Toriyama K (2009) Suppressed expression of RETROGRADE-REGULATED MALE STERILITY restores pollen fertility in cytoplasmic male sterile rice plants. Proc Natl Acad Sci USA 106:9513–9518CrossRefPubMedPubMedCentralGoogle Scholar
  18. Gallagher LJ, Betz SK, Chase CD (2002) Mitochondrial RNA editing truncates a chimeric open reading frame associated with S male-sterility in maize. Curr Genet 42:179–184CrossRefPubMedGoogle Scholar
  19. Geisler DA, Päpke C, Obata T, Nunes-Nesi A, Matthes A, Schneitz K, Maximova E et al (2012) Down regulation of the δ-subunit reduces mitochondrial ATP synthase levels, alters respiration, and restricts growth and gametophyte development in Arabidopsis. Plant Cell 24:2792–2811CrossRefPubMedPubMedCentralGoogle Scholar
  20. Hanson MR, Bentolila S (2004) Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16:S154–S169CrossRefPubMedPubMedCentralGoogle Scholar
  21. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8:R19CrossRefPubMedPubMedCentralGoogle Scholar
  22. Hill TA, Day CD, Zondlo SC, Thackeray AG, Irish VF (1998) Discrete spatial and temporal cis-acting elements regulate transcription of the Arabidopsis floral homeotic gene APETALA3. Development 125:1711–1721PubMedGoogle Scholar
  23. Holec S, Lange H, Kuhn K, Alioua M, Borner T, Gagliardi D (2006) Relaxed transcription in Arabidopsis mitochondria is counter balanced by RNA stability control mediated by poly-adenylation and polynucleotide phosphorylase. Mol Cell Biol 26:2869–2876CrossRefPubMedPubMedCentralGoogle Scholar
  24. Howad W, Tang HV, Pring DR, Kempken F (1999) Nuclear genes from T× CMS maintainer lines are unable to maintain atp6 editing in any anther cell-type in the Sorghum bicolor A3 cytoplasm. Curr Genet 36:62–68CrossRefPubMedGoogle Scholar
  25. Hu J, Wang K, Huang W, Liu G, Gao Y, Wang J, Huang Q et al (2012) The rice pentatricopeptide repeat protein RF5 restores fertility in Hong-Lian cytoplasmic male-sterile lines via a complex with the glycine-rich protein GRP162. Plant Cell 24:109–122CrossRefPubMedPubMedCentralGoogle Scholar
  26. Igarashi K, Kazama T, Motomura K, Toriyama K (2013) Whole genomic sequencing of RT98 mitochondria derived from Oryza rufipogon and northern blot analysis to uncover a cytoplasmic male sterility-associated gene. Plant Cell Physiol 54:237–243CrossRefPubMedGoogle Scholar
  27. Ito T, Ng KH, Lim TS, Yu H, Meyerowitz EM (2007) The homeotic protein AGAMOUS controls late stamen development by regulating a jasmonate biosynthetic gene in Arabidopsis. Plant Cell 19:3516–3529CrossRefPubMedPubMedCentralGoogle Scholar
  28. Iwabuchi M, Kyozuka J, Shimamoto K (1993) Processing followed by complete editing of an altered mitochondrial apt6 RNA restores fertility of cytoplasmic male sterile rice. EMBO J 12:1437–1446PubMedPubMedCentralGoogle Scholar
  29. Iwabuchi M, Koizuka N, Fujimoto H, Sakai T, Imamura J (1999) Identification and expression of the kosena radish (Raphanus sativus cv. Kosena) homologue of the ogura radish CMS-associated gene, orf138. Plant Mol Biol 39:183–188CrossRefPubMedGoogle Scholar
  30. Jing B, Heng S, Tong D, Wan Z, Fu T, Tu J, Ma C et al (2011) A male sterility associated cytotoxic protein ORF288 in Brassica juncea causes aborted pollen development. J Exp Bot 63:1285–1295CrossRefPubMedPubMedCentralGoogle Scholar
  31. Kim DH, Kang JG, Kim B-D (2007) Isolation and characterization of the cytoplasmic male sterility-associated orf456 gene of chili pepper (Capsicum annuum L.). Plant Mol Biol 63:519–532CrossRefPubMedGoogle Scholar
  32. Köhler RH, Horn R, Lössl A, Zetsche K (1991) Cytoplasmic male sterility in sunflower is correlated with the co-transcription of a new open reading frame with the atpA gene. Mol Gen Genet 227:369–376CrossRefPubMedGoogle Scholar
  33. Köhler RH, Cao J, Zipfel WR, Webb WW, Hanson MR (1997) Exchange of protein molecules through connections between higher plant plastids. Science 276:2039–2042CrossRefPubMedGoogle Scholar
  34. Krishnasamy S, Makaroff CA (1993) Characterization of the radish mitochondrial orfB locus, possible relationship with male sterility in Ogura radish. Curr Genet 24:156–163CrossRefPubMedGoogle Scholar
  35. Kurek I, Ezra D, Begu D, Erel N, Litvak S, Breiman A (1997) Studies on the effects of nuclear background and tissue specificity on RNA editing of the mitochondrial ATP synthase subunits α, 6 and 9 in fertile and cytoplasmic male-sterile (CMS) wheat. Theor Appl Genet 95:1305–1311CrossRefGoogle Scholar
  36. Landgren M, Zetterstrand M, Sundberg E, Glimelius K (1996) Alloplasmic male-sterile Brassica lines containing B. tournefortii mitochondria express an ORF 3′ of the atp6 gene and a 32 kDa protein. Plant Mol Biol 32:879–890CrossRefPubMedGoogle Scholar
  37. Laver HK, Reynolds SJ, Moneger F, Leaver CJ (1991) Mitochondrial genome organization and expression associated with cytoplasmic male sterility in sunflower (Helianthus annuus). Plant J 1:185–193CrossRefPubMedGoogle Scholar
  38. Li S, Wan C, Kong J, Zhang Z, Li Y, Zhu Y (2004) Programmed cell death during microgenesis in a Honglian CMS line of rice is correlated with oxidative stress in mitochondria. Funct Plant Biol 31:369–376CrossRefGoogle Scholar
  39. Li N, Zhang D-S, Liu H-S, Yin C-S, Li X-X, Liang W-Q, Yuan Z et al (2006) The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18:2999–3014CrossRefPubMedPubMedCentralGoogle Scholar
  40. Li J, Pandeya D, Jo Y-D, Liu W-Y, Kang B-C (2013) Reduced activity of ATP synthase in mitochondria causes cytoplasmic male sterility in chili pepper. Planta 237:1097–1109CrossRefPubMedGoogle Scholar
  41. Liljegren S (2012) Phloroglucinol stain for lignin. Cold Spring Harb Protoc.  https://doi.org/10.1101/pdb.prot4954 Google Scholar
  42. Luo D, Xu H, Liu Z, Guo J, Li H, Chen L, Fang C et al (2013) A detrimental mitochondrial-nuclear interaction causes cytoplasmic male sterility in rice. Nat Genet 45:573–577CrossRefPubMedGoogle Scholar
  43. Mackenzie SA, McIntosh L (1999) Higher plant mitochondria. Plant Cell 11:571–585CrossRefPubMedPubMedCentralGoogle Scholar
  44. Mitsuda N, Iwase A, Yamamoto H, Yoshida M, Seki M, Shinozaki K, Ohme-Takagi M (2007) NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in woody tissues of Arabidopsis. Plant Cell 19:270–280CrossRefPubMedPubMedCentralGoogle Scholar
  45. Niu NN, Liang WQ, Yang XJ, Jin WL, Wilson ZA, Hu JP, Zhang DB (2013) EAT1 promote tapetal cell death by regulating aspartic proteases during male reproductive development in rice. Nat Commun 4:1445CrossRefPubMedGoogle Scholar
  46. Nivison HT, Hanson MR (1989) Identification of a mitochondrial protein associated with cytoplasmic male sterility in petunia. Plant Cell 1:1121–1130CrossRefPubMedPubMedCentralGoogle Scholar
  47. Peng X, Wang K, Hu C, Zhu Y, Wang T, Yang J, Tong J, Li S, Zhu Y (2010) The mitochondrial gene orfH79 plays a critical role in impairing both male gametophyte development and root growth in CMS-Honglian rice. BMC Plant Biol 10:125.  https://doi.org/10.1186/1471-2229-10-125 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Pring DR, Tang HV, Chase CD, Siripant MN (2006) Microspore gene expression associated with cytoplasmic male sterility and fertility restoration in sorghum. Sex Plant Reprod 19:25–35CrossRefGoogle Scholar
  49. Reddy PS, Mahanty S, Kaul T, Nair S, Sopory SK, Reddy MK (2008) A high-throughput genome-walking method and its use for cloning unknown flanking sequences. Anal Biochem 381:248–253CrossRefPubMedGoogle Scholar
  50. Reynolds SM, Käll L, Riffle ME, Bilmes JA, Noble WS (2008) Transmembrane topology and signal peptide prediction using dynamic Bayesian networks. PLoS Comput Biol 4:e1000213.  https://doi.org/10.1371/journal.pcbi.1000213 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Sabar M, Gagliardi D, Balk J, Leaver CJ (2003) ORFB is a subunit of F1F (O)-ATP synthase, insight into the basis of cytoplasmic male sterility in sunflower. EMBO Rep 4:381–386CrossRefPubMedPubMedCentralGoogle Scholar
  52. Saxena KB (2015) From concept to field: evolution of hybrid pigeonpea technology in India. Ind J Genet 75:279–293Google Scholar
  53. Saxena KB, Hingane AJ (2015) Male sterility systems in major field crops and their potential role in crop improvement. In: Plant biology and biotechnology, plant diversity, organization, function and improvement. Springer, New Delhi, pp 639–656Google Scholar
  54. Saxena KB, Kumar RV, Srivastava N, Shiying B (2005) A cytoplasmic-nuclear male-sterility system derived from a cross between Cajanus cajanifolius and Cajanus cajan. Euphytica 145:289–294CrossRefGoogle Scholar
  55. Saxena KB, Ravikoti VK, Dalvi VA, Pandey LB, Gaddikeri G (2010) Development of cytoplasmic nuclear male sterility, its inheritance, and potential use in hybrid pigeonpea breeding. J Hered 101:497–503CrossRefPubMedGoogle Scholar
  56. Saxena KB, Sameerkumar CV, Hingane AJ, Nagesh Kumar MV, Vijaykumar RA, Saxena RK, Patil S, Varshney RK (2016) Hybrid ICPH 2740 assures quantum jump in pigeonpea productivity in peninsular India. J Food Legum 29:142–144Google Scholar
  57. Schnable PS, Wise RP (1998) The molecular basis of cytoplasmic male sterility and fertility restoration. Trends Plant Sci 3:175–180CrossRefGoogle Scholar
  58. Sinha P, Saxena KB, Saxena RK, Singh VK, Suryanarayana V, Sameerkumar CV, Katta MAVS. et al (2015) Association of nad7a gene with cytoplasmic male sterility in pigeonpea (Cajanus cajan). Plant Genome 8:1–12CrossRefGoogle Scholar
  59. Sorensen AM, Kröber S, Unte US, Huijser P, Dekker K, Saedler H (2003) The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor. Plant J 33:413–423CrossRefPubMedGoogle Scholar
  60. Steiner-Lange S, Unte US, Eckstein L, Yang C, Wilson ZA, Schmelzer E, Dekker K, Saedler H (2003) Disruption of Arabidopsis thaliana MYB26 results in male sterility due to non-dehiscent anthers. Plant J 34:519–528CrossRefPubMedGoogle Scholar
  61. Sunkara S, Bhatnagar-Mathur P, Sharma KK (2013) Isolation and functional characterization of two novel seed specific promoters from legumes. Appl Biochem Biotechnol 172:325–339CrossRefGoogle Scholar
  62. Tang HV, Pring DR, Shaw LC, Salazar RA, Muza FR, Yan B, Schertz KF (1996) Transcript processing internal to a mitochondrial open reading frame is correlated with fertility restoration in male-sterile sorghum. Plant J 10:123–133CrossRefPubMedGoogle Scholar
  63. Tang HV, Chen W, Pring DR (1999) Mitochondrial orf107 transcription, editing, and nucleolytic cleavage conferred by the gene Rf3 are expressed in sorghum pollen. Sex Plant Reprod 12:53–59CrossRefGoogle Scholar
  64. Thevenin J, Pollet B, Letarnec B, Saulnier L, Gissot L, Maia-Grondard A, Lapierre C, Jouanin L (2011) The simultaneous repression of CCR and CAD, two enzymes of the lignin biosynthetic pathway, results in sterility and dwarfism in Arabidopsis thaliana. Mol Plant 4:70–82CrossRefPubMedGoogle Scholar
  65. Tuteja R, Saxena RK, Davila J, Shah T, Chen W, Xiao Y-L, Fan G et al (2013) Cytoplasmic male sterility-associated chimeric open reading frames identified by mitochondrial genome sequencing of four Cajanus genotypes. DNA Res 20:485–495CrossRefPubMedPubMedCentralGoogle Scholar
  66. Vizcay-Barrena G, Wilson ZA (2006) Altered tapetal PCD and pollen wall development in the Arabidopsis ms1 mutant. J Exp Bot 57:2709–2717CrossRefPubMedGoogle Scholar
  67. Wang Z, Zou Y, Li X, Zhang Q, Chen L, Wu H, Su D et al (2006) Cytoplasmic male sterility of rice with boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing. Plant Cell 18:676–687CrossRefPubMedPubMedCentralGoogle Scholar
  68. Wen L, Ruesch KL, Ortega VM, Kamps TL, Gabay-Laughnan S, Chase CD (2003) A nuclear restorer-of-fertility mutation disrupts accumulation of mitochondrial ATP synthase subunit alpha in developing pollen of S male-sterile maize. Genetics 165:771–779PubMedPubMedCentralGoogle Scholar
  69. Wilson ZA, Zhang DB (2009) From Arabidopsis to rice: pathways in pollen development. J Exp Bot 60:1479–1492CrossRefPubMedGoogle Scholar
  70. Wilson ZA, Morroll SM, Dawson J, Swarup R, Tighe PJ (2001) The Arabidopsis MALE STERILITY1 (MS1) gene is a transcriptional regulator of male gametogenesis, with homology to the PHD-finger family of transcription factors. Plant J 28:27–39CrossRefPubMedGoogle Scholar
  71. Xiao H, Zhang F, Zheng Y (2006) The 5′ stem-loop and its role in mRNA stability in maize S cytoplasmic male sterility. Plant J 47:864–872CrossRefPubMedGoogle Scholar
  72. Xu P, Yang Y, Zhang Z, Chen W, Zhang C, Zhang L, Zou S, Ma Z (2008) Expression of the nuclear gene TaF(A)d is under mitochondrial retrograde regulation in anthers of male sterile wheat plants with timopheevii cytoplasm. J Exp Bot 59:1375–1381CrossRefPubMedGoogle Scholar
  73. Xu J, Yang CY, Yuan Z, Zhang DS, Gondwe MY, Ding ZW, Liang W, Zhang D, Wilson ZA (2010) The ABORTED MICROSPORES regulatory network is required for post-meiotic male reproductive development in Arabidopsis thaliana. Plant Cell 22:91–107CrossRefPubMedPubMedCentralGoogle Scholar
  74. Yamamoto MP, Shinada H, Onodera Y, Komaki C, Mikami T, Kubo T (2008) A male sterility-associated mitochondrial protein in wild beets causes pollen disruption in transgenic plants. Plant J 54:1027–1036CrossRefPubMedGoogle Scholar
  75. Yang C, Xu Z, Song J, Conner K, Vizcay-Barrena G, Wilson ZA (2007) Arabidopsis MYB26/MALE STERILE35 regulates secondary thickening in the endothecium and is essential for anther dehiscence. Plant Cell 19:534–548CrossRefPubMedPubMedCentralGoogle Scholar
  76. Yang J, Liu X, Yan X, Zhang M (2010) Mitochondrially-targeted expression of a cytoplasmic male sterility-associated orf220 gene causes male sterility in Brassica juncea. BMC Plant Biol 10:231CrossRefPubMedPubMedCentralGoogle Scholar
  77. Yoshimi M, Kitamura Y, Isshiki S, Saito T, Yasumoto K, Terachi T, Yamagishi H (2013) Variations in the structure and transcription of the mitochondrial atp and cox genes in wild Solanum species that induce male sterility in eggplant (S. melongina). Theor Appl Genet 126:1851–1859CrossRefPubMedGoogle Scholar
  78. Young EG, Hanson MR (1987) A fused mitochondrial gene associated with cytoplasmic male sterility is developmentally regulated. Cell 50:41–49CrossRefPubMedGoogle Scholar
  79. Zhang W, Sun YJ, Timofejeva L, Chen CB, Grossniklaus U, Ma H (2006) Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor. Development 133:3085–3095CrossRefPubMedGoogle Scholar
  80. Zhang D-S, Liang W-Q, Yuan Z, Li N, Shi J, Wang J, Liu Y-M, Zhang D-B (2008) Tapetum degeneration retardation is critical for aliphatic metabolism and gene regulation during rice pollen development. Mol Plant 1:599–610CrossRefPubMedGoogle Scholar
  81. Zhang DB, Luo X, Zhu L (2011) Cytological analysis and genetic control of rice anther development. J Genet Genomics 38:379–390CrossRefPubMedGoogle Scholar
  82. Zhu J, Chen H, Li H, Gao JF, Jiang H, Wang C, Guan YF, Yang ZN (2008) Defective in tapetal development and function 1 is essential for anther development and tapetal function for microspore maturation in Arabidopsis. Plant J 55:266–277CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.International Crops Research Institute for the Semi-Arid Tropics (ICRISAT)HyderabadIndia

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