Abstract
Intracellular signaling pathways between the mitochondria and the nucleus are important in both normal and abnormal development in plants. The homeotic transformation of stamens into pistil-like structures (a phenomenon termed pistillody) in cytoplasmic substitution (alloplasmic) lines of bread wheat (Triticum aestivum) has been suggested to be induced by mitochondrial retrograde signaling, one of the forms of intracellular communication. We showed previously that the mitochondrial gene orf260 could alter the expression of nuclear class B MADS-box genes to induce pistillody. To elucidate the interactions between orf260 and nuclear homeotic genes, we performed a microarray analysis to compare gene expression patterns in the young spikes of a pistillody line and a normal line. We identified five genes that showed higher expression levels in the pistillody line. Quantitative expression analysis using real-time PCR indicated that among these five genes, Wheat Calmodulin-Binding Protein 1 (WCBP1) was significantly upregulated in young spikes of the pistillody line. The amino acid sequence of WCBP1 was predicted from the full-length cDNA sequence and found to encode a novel plant calmodulin-binding protein. RT-PCR analysis indicated that WCBP1 was preferentially expressed in young spikes at an early stage and decreased during spike maturation, indicating that it was associated with spikelet/floret development. Furthermore, in situ hybridization analysis suggested that WCBP1 was highly expressed in the pistil-like stamens at early to late developmental stages. These results indicate that WCBP1 plays a role in formation and development of pistil-like stamens induced by mitochondrial retrograde signaling.
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Abbreviations
- CaM:
-
Calmodulin
- CMS:
-
Cytoplasmic male sterility
- Ctg:
-
Contig
- CS:
-
Chinese Spring
- MRS:
-
Mitochondrial retrograde signaling
- N26:
-
Norin 26
References
Akama K, Akihiro T, Kitagawa M, Takaiwa F (2001) Rice (Oryza sativa) contains a novel isoform of glutamate decarboxylase that lacks an authentic calmodulin-binding domain at the C-termius. Biochim Biophys Acta 1522:143–150
Alexandrov NN, Brover VV, Freidin S, Troukhan ME, Tatarinova TV, Zhang H, Swaller TJ, Lu YP, Bouck J, Flavell RB, Feldmann KA (2009) Insights into corn genes derived from large-scale cDNA sequencing. Plant Mol Biol 69:179–194
Ambrose BA, Lerner DR, Ciceri P, Padilla CM, Yanofsky MF, Schmidt RJ (2000) Molecular and genetic analyses of the Silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Mol Cell 5:569–579
Arazi T, Sunkar R, Kaplan B, Fromm H (1999) A tobacco plasma membrane calmodulin-binding transporter confers Ni2+ tolerance and Pb2+ hypersensitivitiy in transgenic plants. Plant J 20:171–182
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc (ser B [Methodol]) 57:289–300
Butow RA, Avadhani NG (2004) Mitochondrial signaling: the retrograde response. Mol Cell 14:1–15
Campbell JL, Klueva NY, Zheng HG, Nieto-Sotelo J, Ho TD, Nguyen HT (2001) Cloning of new members of heat shock protein HSP101 gene family in wheat (Triticum aestivum (L.) Moench) inducible by heat, dehydration, and ABA(1). Biochim Biophys Acta 1517:270–277
Chae E, Tan QK-G, Hill TA, Irish VF (2008) An Arabidopsis F-box protein acts as a transcriptional co-factor to regulate floral development. Development 135:1235–1245
Chase CD (2007) Cytoplasmic male sterility: a window to the world of plant mitochondrial-nuclear interactions. Trends Genet 23:81–90
Choi MS, Kim MC, Yoo JH, Moon BC, Koo SC, Park BO, Lee JH, Koo YD, Han HJ, Lee SY, Chung WS, Lim CO, Cho MJ (2005) Isolation of a calmodulin-binding transcription factor from rice (Oryza sativa L.). J Biol Chem 280:40821–40831
Chung WS, Lee SH, Kim JC, Do-Heo W, Kim MC, Park CY, Park HC, Lim CO, Kim WB, Harper JF, Cho MJ (2000) Identification of a calmodulin-regulated soybean Ca(2+)-ATPase (SCA1) that is located in the plasma membrane. Plant Cell 12:1393–1407
Fujii S, Toriyama K (2008) Genome barriers between nuclei and mitochondria exemplified by cytoplasmic male sterility. Plant Cell Physiol 49:1484–1494
Goto K, Meyerowitz EM (1994) Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev 8:1548–1560
Hama E, Takumi S, Ogihara Y, Murai K (2004) Pistillody is caused by alterations to the class-B MADS-box gene expression pattern in alloplasmic wheats. Planta 218:712–720
Hanson MR, Bentolila S (2004) Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16:S154–S169
Hua W, Liang S, Lu YT (2003) A tobacco (Nicotiana tabaccum) calmodulin-binding protein NtCBK2, is regulated differentially by calmodulin isoforms. Biochem J 376:291–302
Jack T, Brockman LL, Meyerowitz EM (1992) The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell 68:683–697
Johnson KG, Kornfeld K (2010) The CRAL/TRIO and GOLD domain protein TAP-1 regulates RAF-1 activation. Dev Biol 341:464–471
Kaul MLH (1988) Male sterility in higher plant. Monographs Theor Appl Genet, vol 10. Springer, Berlin
Kawaura K, Mochida K, Ogihara Y (2005) Expression profile of two storage-protein gene families in hexaploid wheat revealed by large-scale analysis of expressed sequence tags. Plant Physiol 139:1870–1880
Kawaura K, Mochida K, Yamazaki Y, Ogihara Y (2006) Transcriptome analysis of salinity stress responses in common wheat using 22k oligo-DNA microarray. Funct Integr Genomics 6:132–142
Kawaura K, Mochida K, Ogihara Y (2008) Genome-wide analysis for identification of salt-responsive genes in common wheat. Funct Integr Genomics 8:277–286
Kawaura K, Mochida K, Enju A, Totoki Y, Toyoda A, Sakaki Y, Kai C, Kawai J, Hayashizaki Y, Seki M, Shinozaki K, Ogihara K (2009) Assessment of adaptive evolution between wheat and rice as deduced from full-length common wheat cDNA sequence data and expression patterns. BMC Genomics 10:271
Kim MC, Chung WS, Yun D-J, Cho MJ (2009) Calcium and calmodulin-mediated regulation of gene expression in plants. Mol Plant 2:13–21
Kinjo H, Shitsukawa N, Takumi S, Murai K (2012) Diversification of three APETALA1/FRUITFULL-like genes in wheat. Mol Genet Genomics 287:283–294
Kofer W, Glimelius K, Bonnett HT (1991) Modifications of mitochondrial DNA cause changes in floral development in homeotic-like mutants of tobacco. Plant Cell 3:759–769
Kuroda H, Takahashi N, Shimada H, Seki M, Shinozaki K, Matsui M (2002) Classification and expression analysis of Arabidopsis F-Box-containing protein genes. Plant Cell Physiol 43:1073–1085
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948
Leino M, Teixeira R, Landgren M, Glimelius K (2003) Brassica napus lines with rearranged Arabidopsis mitochondria display CMS and a range of developmental aberrations. Theor Appl Genet 106:1156–1163
Linke B, Nothnagel T, Borner T (1999) Morphological characterization of modified flower morphology of three novel alloplasmic male sterile carrot sources. Plant Breed 118:543–548
Linke B, Nothnagel T, Borner T (2003) Flower development in carrot CMS plants: mitochondria affect the expression of MADS box genes homologous to GLOBOSA and DEFICIENS. Plant J 34:27–37
Liu Z, Butow RA (2006) Mitochondrial retrograde signaling. Annu Rev Genet 40:159–185
Lu YT, Dharmasiri MA, Harrington HM (1995) Characterization of a cDNA encoding a novel heat-shock protein that binds to calmodulin. Plant Physiol 108:1197–1202
Ma L, Liang S, Jones RL, Lu YT (2004) Characterization of a novel calcium/calmodulin-dependent kinase from tobacco. Plant Physiol 135:1280–1293
Murai K, Tsunewaki K (1993) Photoperiod-sensitive cytoplasmic male sterility in wheat with Aegilops crassa cytoplasm. Euphytica 67:41–48
Murai K, Tsunewaki K (1994) Genetic analysis on the fertility restoration by Triticum aestivum cv. Chinese Spring against photoperiod-sensitive cytoplasmic male sterility. Jpn J Genet 69:195–202
Murai K, Murai R, Takumi S, Ogihara Y (1998) Cloning and characterization of cDNAs corresponding to the wheat MADS box genes. Proc 9th Int Wheat Genet Symp 1:89–94
Murai K, Takumi S, Koga H, Ogihara Y (2002) Pistillody, homeotic transformation of stamens into pistil-like structures, caused by nuclear-cytoplasm interaction in wheat. Plant J 29:169–181
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 159:315–323
Nagasawa N, Miyoshi M, Sano Y, Satoh H, Hirano H-Y, Sakai H, Nagato Y (2003) SUPERWOMAN1 and DROOPING LEAF genes control floral organ identity in rice. Development 130:705–718
Ogihara Y, Mochida K, Kawaura K, Murai K, Seki M, Kamiya A, Shinozaki K, Carninci P, Hayashizaki Y, Shin-I T, Kohara Y, Yamazaki Y (2004) Construction of a full-length cDNA library from young spikelets of hexaploid wheat and its characterization by large-scale sequencing of expressed sequence tags. Genes Genet Syst 79:227–232
Ranty B, Aldon D, Galaud J-P (2006) Plant calmodulins and calmodulin-related proteins. Plant Signal Behav 1:96–104
Reddy VS, Ali GS, Reddy ASN (2002) Genes encoding calmodulin-binding proteins in the Arabidopsis genome. J Biol Chem 277:9840–9852
Riechmann JL, Meyerowitz EM (1997) MADS domain proteins in plant development. Biol Chem 378:1079–1101
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Saraike T, Shitsukawa N, Yamamoto Y, Hagita H, Iwasaki Y, Takumi S, Murai K (2007) Identification of a protein kinase gene associated with pistillody, homeotic transformation of stamens into pistil-like structures, in alloplasmic wheat. Planta 227:211–221
Schuurink RC, Shartzer SF, Fath A, Jones RL (1998) Characterization of a calmodulin-binding transporter from the plasma membrane of barley aleurone. Proc Natl Acad Sci USA 95:1944–1949
Shitsukawa N, Kinjo H, Takumi S, Murai K (2009) Heterochronic development of the floret meristem determines grain number per spikelet in diploid, tetraploid and hexaploid wheats. Ann Bot 104:243–251
Sommer H, Beltran J-P, Huijser P, Pape H, Lönnig W-E, Saedler H, Schwarz-Sommer Z (1990) Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus: the protein shows homology to transcription factors. EMBO J 9:605–613
Stael S, Wurzinger B, Mair A, Mehlmer N, Vothknecht UC, Teige M (2012) Plant organellar calcium signaling: an emerging field. J Exp Bot 63:1525–1542
Subbaiah CC, Sachs MM (2000) Maize cap1 encodes a novel SERCA-type calcium-ATPase with a calmodulin-binding domain. J Biol Chem 275:21678–21687
Szabadkai G, Duchen MR (2008) Mitochondria: the hub of cellular Ca2+ signaling. Physiology 23:84–94
Tang J, Ohyama K, Kawaura K, Hashinokuchi H, Kamiya Y, Suzuki M, Muranaka T, Ogihara Y (2011) A new insight into application for barley chromosome addition lines of common wheat: achievement of stigmasterol accumulation. Plant Physiol 157:1555–1567
Teixeira RT, Farbos I, Glimelius K (2005) Expression levels of meristem identity and homeotic genes are modified by nuclear-mitochondrial interactions in alloplasmic male-sterile lines of Brassica napus. Plant J 42:731–742
Tröbner W, Ramirez L, Motte P, Hue I, Huijser P, Lönnig W-E, Saedler H, Sommer H, Schwarz-Sommer Z (1992) GLOBOSA: a homeotic gene which interacts with DEFICIENS in the control of Antirrhinum floral organogenesis. EMBO J 11:4693–4704
Tsunewaki K, Wang G-Z, Matsuoka Y (1996) Plasmon analysis of Triticum (wheat) and Aegilops. 1. Production of alloplasmic common wheats and their fertilities. Genes Genet Syst 71:293–311
Tsunewaki K, Wang G-Z, Matsuoka Y (2002) Plasmon analysis of Triticum (wheat) and Aegilops. 2. Characterization and classification of 47 plasmons based on their effects on common wheat phenotype. Genes Genet Syst 77:409–427
Wang W, Takezawa D, Narasimhulu SB, Reddy AS, Poovaiah BW (1996) A novel kinesin-like protein with a calmodulin-binding domain. Plant Mol Biol 31:87–100
Yang T, Poovaiah BW (2000) An early ethylene up-regulated gene encoding a calmodulin-binding protein involved in plant senescence and death. J Biol Chem 275:38467–38473
Yang T, Peng H, Whitaker BD, Conway WS (2012) Characterization of a calcium/calmodulin-regulated SR/CAMTA gene family during tomato fruit development and ripening. BMC Plant Biol 12:19
Zahn LN, Feng B, Ma H (2006) Beyond the ABC-model: regulation of floral homeotic genes. In: Soltis DE, Leebens-Mack JH, Soltis PS (eds) Developmental genetics of the flower. Adv Bot Res 44:163–207
Zegzouti H, Jones B, Frasse P, Marty C, Maitre B, Latch A, Pech JC, Bouzayen M (1999) Ethylene-regulated gene expression in tomato fruit: characterization of novel ethylene-responsive and ripening-related genes isolated by differential display. Plant J 18:589–600
Zhu Y, Saraike T, Yamamoto Y, Hagita H, Takumi S, Murai K (2008) orf260 cra, a novel mitochondrial gene, is associated with the homeotic transformation of stamens into pistil-like structures (pistillody) in alloplasmic wheat. Plant Cell Phsyol 49:1723–1733
Zielinski RE (1998) Calmodulin and calmodulin-binding proteins in plants. Annu Rev Plant Physiol Mol Biol 49:697–725
Zubko MK (2004) Mitochondrial tuning fork in nuclear homeotic functions. Trends Plant Sci 9:61–64
Zubko MK, Zubko EI, Patskovsky YV, Khvedynich OA, Fisahn J, Gleba YY, Schieder O (1996) Novel ‘homeotic’ CMS patterns generated in Nicotiana via cybridization with Hyoscyamus and Scopolia. J Exp Bot 47:1101–1110
Zubko MK, Zubko EI, Ruban AV, Adler K, Mock H-P, Misera S, Gleba YY, Grimm B (2001) Extensive developmental and metabolic alterations in cybrids Nicotiana tabacum (+Hyoscyamus niger) are caused by complex nucleo-cytoplasmic incompatibility. Plant J 25:627–639
Acknowledgments
We are grateful to the National Bioresource Project—Wheat (NBRP–KOMUGI) for providing wheat materials. This work was supported in part by a Grant-in-Aid for Scientific Research (B) (No. 21380009) and a Grant-in-Aid for Scientific Research on Innovative Area (No. 24113517) from the Ministry of Education, Science and Culture of Japan (to K. M.).
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The nucleotide sequence for WCBP1 cDNA reported in this paper has been submitted to the DDBJ/EMBL/GenBank database under the accession number AB716956. The wheat oligomicroarray with 37,826 probes is registered as GPL9805 in GEO at NCBI. A complete set of microarray data from this study was deposited to the GEO repository under the accession number GSM920888-920891.
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Yamamoto, M., Shitsukawa, N., Yamada, M. et al. Identification of a novel homolog for a calmodulin-binding protein that is upregulated in alloplasmic wheat showing pistillody. Planta 237, 1001–1013 (2013). https://doi.org/10.1007/s00425-012-1812-x
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DOI: https://doi.org/10.1007/s00425-012-1812-x