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Journal of Integrative Agriculture  2016, Vol. 15 Issue (10): 2183-2191    DOI: 10.1016/S2095-3119(15)61190-X
Crop Genetics · Breeding · Germplasm Resources Advanced Online Publication | Current Issue | Archive | Adv Search |
Experimental and genomic evidence for the indica-type cytoplasmic effect in Oryza sativa L. ssp. japonica
LIU You-hong*, TANG Liang*, XU Quan*, MA Dian-rong, ZHAO Ming-hui, SUN Jian, CHEN Wen-fu
Rice Research Institute, Shenyang Agricultural University/Key Laboratory of Northern japonica Rice Genetics and Breeding, Ministry of Education and Liaoning Province/Key Laboratory of Northeast Rice Biology and Genetics and Breeding, Ministry of Agriculture/Collaborative Innovation Center of japonica Rice Genetic Improvement and Production in Northeast China, Shenyang 110866, P.R.China
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Abstract      Cytoplasmic effects are important agronomical phenomena that have generated widespread interest in both theory and application. In the present study, five high yield rice cultivars (Oryza sativa L. ssp. japonica) in large-scale cultivation in northeast China were determined to possess Oryza sativa L. ssp. indica-type cytoplasm using cytoplasmic subspecies-specific molecular markers. This was confirmed by cytoplasmic genome-wide single nucleotide polymorphisms (SNPs) and functional gene sequencing. Two of these five japonica cultivars were core breeding parents with high yield and the other three were super-high-yield varieties registered by the Ministry of Agriculture of China. We constructed nuclear substitution lines to further demonstrate whether and how this indica-type cytoplasm contributed to yield improvement by comparing yield components. The results showed that under the same japonica nuclear background, the lines with indica-type cytoplasm had a significant decrease in tillers in exchange for increased grain number per panicle compared with their recurrent parents. Our results implied that botanical basis of this cytoplasmic effect was to reduce the plant’s branching differentiation to produce more floral organs under the constant nutrition. Our findings open another door for the utilization of inter-subspecific hybridization for the improvement of rice cultivar.
Keywords:  cytoplasmic effects        cytoplasmic genome-wide SNPs        super high yield rice        nuclear substitution lines  
Received: 07 September 2015   Accepted:
Fund: 

This study was supported by the National Natural Science Foundation of China (31371587 and 31430062), the Cultivation Plan for Youth Agricultural Science and Technology Innovative Talents of Liaoning Province (2014046), the China Postdoctoral Science Foundation Grant (2014M560221) and the Program for Changjiang Scholars and Innovative Research Team in University (PCSIRT), China.

Corresponding Authors:  SUN Jian, E-mail: as_1230@163.com; CHEN Wen-fu, Tel/Fax: +86-24-88487184, E-mail: wfchen5512@126.com    
About author:  LIU You-hong, E-mail: liuyouhong1011@126.com;

Cite this article: 

LIU You-hong, TANG Liang, XU Quan, MA Dian-rong, ZHAO Ming-hui, SUN Jian, CHEN Wen-fu. 2016. Experimental and genomic evidence for the indica-type cytoplasmic effect in Oryza sativa L. ssp. japonica. Journal of Integrative Agriculture, 15(10): 2183-2191.

Atienza S, Martin A, Ramirez M, Martin A, Ballesteros J. 2007. Effects of Hordeum chilense cytoplasm on agronomic traits in common wheat. Plant Breeding, 126, 5–8.

Chandra-Shekara A, Prasanna B, Singh B, Unnikrishnan K, Seetharam A. 2007. Effect of cytoplasm and cytoplasm-nuclear interaction on combining ability and heterosis for agronomic traits in pearl millet {Pennisetum glaucum (L) Br. R}. Euphytica, 153, 15–26.

Christensen A C. 2013. Plant mitochondrial genome evolution can be explained by DNA repair mechanisms. Genome Biology and Evolution, 5, 1079–1086.

Evanno G, Regnaut S, Goudet J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611–2620.

Galloway L F, Fenster C B. 1999. The effect of nuclear and cytoplasmic genes on fitness and local adaptation in an annual legume, Chamaecrista fasciculata. Evolution, 53, 1734–1743.

Gökçe A F, Havey M J. 2006. Selection at the Ms locus in open pollinated onion (Allium cepa L.) populations possessing S-cytoplasm or mixtures of N- and S-cytoplasms. Genetic Resources and Crop Evolution, 53, 1495–1499.

Galtier N. 2011. The intriguing evolutionary dynamics of plant mitochondrial DNA. BMC Biology, 9, 61.

Garris A J, Tai T H, Coburn J, Kresovich S, McCouch S. 2005. Genetic structure and diversity in Oryza sativa L. Genetics. 169, 1631–1638.

Howe C J. 2012. Chloroplast genome. In: Encyclopedia of Life Sciences (ELS). John Wiley & Sons, Chichester.

Huang J, Cai M, Long Q, Liu L, Lin Q, Jiang Chen S, Wan J. 2014. OsLOX2, a rice type I lipoxygenase, confers opposite effects on seed germination and longevity. Transgenic Research, 23, 643–655.

Hu J, Wang K, Huang W, Liu G, Gao Y, Wang J, Huang Q, Ji Y, Qin X, Wan L. 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. The Plant Cell, 24, 109–122.

Kanno A, Watanabe N, Nakamura I, Hirai A. 1993. Variations in chloroplast DNA from rice (Oryza sativa): Differences between deletions mediated by short direct-repeat sequences within a single species. Theoretical and Applied Genetics, 86, 579–584.

Kitazaki K, Kubo T. 2010. Cost of having the largest mitochondrial genome: Evolutionary mechanism of plant mitochondrial genome. Journal of Botany, 2010, 1–12.

Kubo T, Newton K J. 2008. Angiosperm mitochondrial genomes and mutations. Mitochondrion, 8, 5–14.

Leon P, Arroyo A, Mackenzie S. 1998. Nuclear control of plastid and mitochondrial development in higher plants. Annual Review of Plant Biology, 49, 453–480.

Li R, Yu C, Li Y, Lam T W, Yiu S M, Kristiansen K, Wang J. 2009. SOAP2: An improved ultrafast tool for short read alignment. Bioinformatics, 25, 1966–1967.

Liu D, Ma C, Hong W, Huang L, Liu M, Liu H, Zheng H, Deng D, Xin H, Song J. 2014. Construction and analysis of high-density linkage map using high-throughput sequencing data. PLOS ONE, 6, e98855.

Liu K, Muse S V. 2005. PowerMarker: An integrated analysis environment for genetic marker analysis. Bioinformatics, 21, 2128–2129.

Luo D, Xu H, Liu Z, Guo J, Li H, Chen L, Fang C, Zhang Q, Bai M, Yao N. 2013. A detrimental mitochondrial-nuclear interaction causes cytoplasmic male sterility in rice. Nature Genetics, 45, 573–577.

Mizumoto K, Murai K, Nakamura C, Takumi S. 2004. Preferential expression of a homolog encoding a mitochondrial L14 ribosomal protein in stamens of common wheat. Gene, 343, 281–289.

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. The Plant Journal, 29, 169–181.

Nakamura I, Urairong H, Kameya N, Fukuta Y, Chitrakon S, Sato Y. 1998. Six different plastid subtypes were found in O. sativa-O. rufipogon complex. Rice Genetics Newsletter, 15, 80–81.

Nott A, Jung H S, Koussevitzky S, Chory J. 2006. Plastid-to-nucleus retrograde signaling. Annual Review of Plant Biology, 57, 739–759.

Ramana S, Sharma-Natu P, Ghildiyal M C. 2002. Cytoplasmic effects on photosynthesis and ribulose-1,5-bisphosphate carboxylase activity in Brassica species. Euphytica, 123, 361–365.

Rao A, Fleming A. 1978. Cytoplasmic-genotypic effects in the GT 112 maize inbred with four cytoplasms. Crop Science, 18, 935–937.

Rao Y, Li Y, Qian Q. 2014. Recent progress on molecular breeding of rice in China. Plant Cell Reports, 33, 551–564.

Shi Y, Liu X, Li R, Gao Y, Xu Z, Zhang B, Zhou Y. 2014. Retention of OsNMD3 in the cytoplasm disturbs protein synthesis efficiency and affects plant development in rice. Journal of Experimental Botany, 65, 3055–3069.

Strand Å. 2004. Plastid-to-nucleus signalling. Current Opinion in Plant Biology, 7, 621–625.

Sun J, Liu D, Wang J Y, Ma D R, Tang L, Gao H, Xu Z J, Chen W F. 2012. The contribution of intersubspecific hybridization to the breeding of super-high-yielding japonica rice in northeast China. Theoretical and Applied Genetics, 125, 1149–1157.

Sun J, Qian Q, Ma D R, Xu Z J, Liu D, Du H B, Chen W F. 2013. Introgression and selection shaping the genome and adaptive loci of weedy rice in northern China. New Phytologist, 197, 290–299.

Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596–1599.

Tang J, Xia H A, Cao M, Zhang X, Zeng W, Hu S, Tong W, Wang J, Wang J, Yu J. 2004. A comparison of rice chloroplast genomes. Plant Physiology, 135, 412–420.

Tao D, Hu F, Yang J, Yang G, Yang Y, Xu P, Li J, Ye C, Dai L. 2004. Cytoplasm and cytoplasm-nucleus interactions affect agronomic traits in japonica rice. Euphytica, 135, 129–134.

Tao D, Xu P, Zhou J, Deng X, Li J, Deng W, Yang J, Yang G, Li Q, Hu F. 2011. Cytoplasm affects grain weight and filled-grain ratio in indica rice. BMC Genetics, 12, 53.

Tian X, Zheng J, Hu S, Yu J. 2006. The rice mitochondrial genomes and their variations. Plant Physiology, 140, 401–410.

Wang Z, Zou Y, Li X, Zhang Q, Chen L, Wu H, Su D, Chen Y, Guo J, Luo D. 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. The Plant Cell, 18, 676–687.

Webber A N, Malkin R. 1990. Photosystem I reaction-centre proteins contain leucine zipper motifs: A proposed role in dimer formation. FEBS Letters, 264, 1–4.

Xu Q, Xu N, Xu H, Tang L, Liu J, Sun J, Wang J. 2014. Breeding value estimation of the application of IPA1 and DEP1 to improvement of Oryza sativa L. ssp. japonica in early hybrid generations. Molecular Breeding, 34, 1933–1942.
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