Chloroplast structure and DNA methylation polymorphisms in an albino mutant of wheat (Triticum aestivum) cv. Xinong 1376
Yulong Song A B D E F G J , Huali Tang A D E F G J , Xiangsheng Ke A , Jialin Guo A D E F G , Shuangxi Zhang C , Junwei Wang A D E F G , Na Niu A D E F G , Shoucai Ma A D E F G , Huiyan Zhao A H I and Gaisheng Zhang A D E F G I
+ Author Affiliations
- Author Affiliations
A College of Agronomy, Northwest A and F University, Yangling, Shaanxi, China.
B State Key Laboratory of Crop Stress Biology for Arid Areas, Yangling, Shaanxi, China.
C Crop Institute of Ningxia Academy of Agricultural and Forestry Science, Yongning, China.
D National Yangling Agricultural Biotechnology and Breeding Center, Yangling, Shaanxi, China.
E Yangling Branch of State Wheat Improvement Center, Yangling, Shaanxi, China.
F Wheat Breeding Engineering Research Center, Ministry of Education, Yangling, Shaanxi, China.
G Key Laboratory of Crop Heterosis of Shaanxi Province, Yangling, Shaanxi, China.
H College of Plant Protection, Northwest A and F University, Yangling, Shaanxi, China.
I Corresponding author. Email: zhanggsh58@aliyun.com; zhaohy@nwsuaf.edu.cn
J These authors contributed equally to this work and should be considered co-first authors.
Crop and Pasture Science 69(4) 362-373 https://doi.org/10.1071/CP17471
Submitted: 13 September 2017 Accepted: 16 January 2018 Published: 16 April 2018
Abstract
DNA methylation plays an important role in regulating plant development, including organ and tissue differentiation, which may determine variations in agronomic traits. However, no reports exist for the regulation of leaf colour in wheat. The present study investigated the chloroplast structure and epigenetic mechanisms regulating leaf colour in an albino mutant of wheat (Triticum aestivum L.) cv. Xinong 1376. Structural analysis was performed by scanning and transmission electron microscopy, and epigenetic modifications were detected by methylation-sensitive amplification polymorphism (MSAP) analysis. Mesophyll cells of green leaves showed a well-ordered arrangement and they were filled with chloroplasts with intact lamellar structures and thylakoid membranes. By contrast, mesophyll cells of red and white leaves were disorganised and contained only a few plastids or chloroplasts with no lamellar structures or thylakoid membranes. Comparison of MSAP profiles revealed that white or red leaves had higher levels of cytosine methylation and showed changes in polymorphic loci compared with green leaves (4.35% and 4.10%, respectively). We sequenced 150 DNA fragments that were differentially displayed in MSAP patterns of white or red and green leaves of the Xinong 1376 albino mutant. A further BLAST search of 77 cloned sequences located them in coding regions. Most of these sequences were found to be involved in processes such as signal transduction, transcription regulation, post-transcriptional processing, DNA modification and repair, transport, biosynthesis of cellulose, photosynthesis, protein ubiquitination, stress responses, and retroposition. Expression analysis demonstrated a decrease in the transcription of two methylated genes, psaA and psbD, which are involved in the photosystem. Although the DNA methylation changes and leaf colour changes were not directly associated, these results may indicate that methylation of specific genes is an active and rapid epigenetic response to variation of leaf colour in the Xinong 1376 albino mutant, further elucidating the mechanism of variation in leaf colour.
Additional keywords: albinism, leaf, methylation, photosynthesis.
References
Ba QS, Zhang GS, Niu N, Ma SC, Wang JW (2014) Cytoplasmic effects on DNA methylation between male sterile lines and the maintainer in wheat (Triticum aestivum L.). Gene 549, 192–197.| Cytoplasmic effects on DNA methylation between male sterile lines and the maintainer in wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht1ektbzF&md5=5c4fd8048f6196605240aec6f1147cbfCAS |
Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annual Review of Plant Biology 59, 89–113.
| Chlorophyll fluorescence: a probe of photosynthesis in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqsL8%3D&md5=f8d026b98dc2126abfc48324c36475e2CAS |
Bewick AJ, Schmitz RJ (2017) Gene body DNA methylation in plants. Current Opinion in Plant Biology 36, 103–110.
| Gene body DNA methylation in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXjt1KgtLs%3D&md5=1662683c87be10918e2798a79b78d077CAS |
Calvin M (1976) Photosynthesis as a resource for energy and materials. Photochemistry and Photobiology 23, 425–444.
| Photosynthesis as a resource for energy and materials.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XlsFKnt7c%3D&md5=d4eb04c58b7882f03aa5401382f9d473CAS |
Campbell BW, Mani D, Curtin SJ, Slattery RA, Michno JM, Ort DR, Schaus PJ, Palmer RG, Orf JH, Stupar RM (2015) Identical substitutions in magnesium chelatase paralogs result in chlorophyll-deficient soybean mutants. G3—Genes Genomes Genetics 5, 123–131.
Candaele J, Demuynck K, Mosoti D, Beemster GTS, Inzé D, Nelissen H (2014) Differential methylation during maize leaf growth targets developmentally regulated genes. Plant Physiology 164, 1350–1364.
| Differential methylation during maize leaf growth targets developmentally regulated genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXkslCltr8%3D&md5=ba8a2a605f20a1e73720d4e2d085657aCAS |
Deng XJ, Zhang HQ, Wang Y, He F, Liu JL, Xiao X, Wang GL (2014) Mapped clone and functional analysis of leaf-color gene ygl7 in a rice hybrid (Oryza sativa L. ssp. indica). PLoS One 9, e99564
| Mapped clone and functional analysis of leaf-color gene ygl7 in a rice hybrid (Oryza sativa L. ssp. indica).Crossref | GoogleScholarGoogle Scholar |
Diner BA, Pappaport F (2002) Structure, dynamics, and energetics of the primary photochemistry of photosystem II of oxygenic photosynthesis. Annual Review of Plant Biology 53, 551–580.
| Structure, dynamics, and energetics of the primary photochemistry of photosystem II of oxygenic photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsVWhu78%3D&md5=9bbf0795a9c25b3a573a12c11cbbb760CAS |
Dong ZY, Wang YM, Zhang ZJ, Shen Y, Lin XY, Ou XF, Han FP, Liu B (2006) Extent and pattern of DNA methylation alteration in rice lines derived from introgressive hybridization of rice and Zizania latifolia Griseb. Theoretical and Applied Genetics 113, 196–205.
| Extent and pattern of DNA methylation alteration in rice lines derived from introgressive hybridization of rice and Zizania latifolia Griseb.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmtFSit70%3D&md5=7fffafade00d63a2c0256796810cc45fCAS |
Dong H, Fei GL, Wu CY, Wu FQ, Sun YY, Chen MJ, Ren YL, Zhou KN, Cheng ZJ, Wang JL, Jiang L, Zhang X, Guo XP, Lei CL, Su N, Wang H, Wan JM (2013) A rice virescent-yellow leaf mutant reveals new insights into the role and assembly of plastid caseinolytic protease in higher plants. Plant Physiology 162, 1867–1880.
| A rice virescent-yellow leaf mutant reveals new insights into the role and assembly of plastid caseinolytic protease in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlWlt73J&md5=cf5379bf86d75bb35ecb6aadd9808ef6CAS |
Falbel TG, Meehl JB, Staehelin JA (1996) Severity of mutant phenotype in a series of chlorophyll-deficient wheat mutants depends on light intensity and the severity of the block in chlorophyll synthesis. Plant Physiology 112, 821–832.
| Severity of mutant phenotype in a series of chlorophyll-deficient wheat mutants depends on light intensity and the severity of the block in chlorophyll synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmsFKkur0%3D&md5=55216521ca3be8951ce3c0a92fc4dad8CAS |
Fang J, Chai CL, Qian Q, Li CL, Tang JY, Sun L, Huang ZJ, Guo XL, Sun CH, Liu M, Zhang Y, Lu QT, Wang YQ, Lu CM, Han B, Chen F, Cheng ZK, Chu CC (2008) Mutations of genes in synthesis of the carotenoid precursors of ABA lead to pre-harvest sprouting and photo-oxidation in rice. The Plant Journal 54, 177–189.
| Mutations of genes in synthesis of the carotenoid precursors of ABA lead to pre-harvest sprouting and photo-oxidation in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlsVWhsr4%3D&md5=f324b5a86ca5b911ffd6a57d0fe07ca4CAS |
Finke A, Rozhon W, Pecinka A (2018) Analysis of DNA methylation content and patterns in plants. Methods in Molecular Biology 1694, 277–298.
| Analysis of DNA methylation content and patterns in plants.Crossref | GoogleScholarGoogle Scholar |
Finnegan EJ, Genger RK, Kovac K, Peacock WJ, Dennis ES (1998) DNA methylation and the promotion of flowering by vernalization. Proceedings of the National Academy of Sciences of the United States of America 95, 5824–5829.
| DNA methylation and the promotion of flowering by vernalization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjtFWrs7s%3D&md5=a95229d0f137f050a99ceab5da018205CAS |
Flavell AJ, Stephen RP, Pat HH, Amar K (1997) The evolution of Ty1-copia group retrotransposons in eukaryote genomes. Genetica 100, 185–195.
| The evolution of Ty1-copia group retrotransposons in eukaryote genomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkslWltg%3D%3D&md5=81d6d2783be22f2b33ed98640731753cCAS |
Gallegos MT, Schleif R, Bairoch A, Hofmann K, Ramos JL (1997) Arac/XylS family of transcriptional regulators. Microbiology and Molecular Biology Reviews 61, 393–410.
Gao ML, Hu LL, Li YH, Weng YQ (2016) The chlorophyll-deficient golden leaf mutation in cucumber is due to a single nucleotide substitution in CsChlI for magnesium chelatase I subunit. Theoretical and Applied Genetics 129, 1961–1973.
| The chlorophyll-deficient golden leaf mutation in cucumber is due to a single nucleotide substitution in CsChlI for magnesium chelatase I subunit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xht1ags7bK&md5=eb59f21ce0f8b32bc7c8670178f027d0CAS |
Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, Dephoure N, O’Shea EK, Weissman JS (2003) Global analysis of protein expression in yeast. Nature 425, 737–741.
| Global analysis of protein expression in yeast.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXotV2iu7c%3D&md5=a081a193d859be3ae0eed276461d097cCAS |
Gong XS, Yan JZ, Wu NH, Yan LF (1992) Molecular cloning and nucleotide sequence of chloroplast psaA gene from sorghum. Chinese Journal of Biotechnology 8, 207–212.
Guo JW, Gu JK, Zhao YR, Du LF (2007) Changes of photosystem II electron transport in the chlorophyll-deficient oilseed rape mutant studied by chlorophyll fluorescence and thermoluminescence. Journal of Integrative Plant Biology 49, 698–705.
| Changes of photosystem II electron transport in the chlorophyll-deficient oilseed rape mutant studied by chlorophyll fluorescence and thermoluminescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlvF2htbs%3D&md5=7f33c6a34a00e05257b9ed4371a7db25CAS |
Hafiz IA (1998) Genomic and DNA methylation variation following transition from juvenile to adult phase in Malus micromalus, Malus hupehensis and Prunus persica seedling trees. PhD Thesis, Dept. of Horticulture, Zhejiang Agriculture University, PR China.
He B, Liu LL, Zhang WW, Wan JM (2006) Plant leaf color mutants. Plant Physiology Journal 42, 1–9.
Henderson IR, Jacobsen SE (2007) Epigenetic inheritance in plants. Nature 447, 418–424.
| Epigenetic inheritance in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlsFOgs78%3D&md5=ea0e3e3f2160c0b37d8b8bf990e93cbfCAS |
Hou DY, Xu H, Du GY, Lin JT, Duan M, Guo AG (2009) Proteome analysis of chloroplast proteins in stage albinism line of winter wheat (Triticum aestivum L.) FA58. BMB Reports 42, 450–455.
| Proteome analysis of chloroplast proteins in stage albinism line of winter wheat (Triticum aestivum L.) FA58.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpvFOlsLY%3D&md5=1cd14f2299d8be6212b6106d6d8a496fCAS |
Hu SY, Xu LF (1990) A cytochemical technique for demonstration of lipid drops, starch and protein bodies in thick resin sections. Journal of Integrative Plant Biology 32, 841–846.
Jeanne ME, Michele R, Pia M, Jacqueline GB, Yves P, Pierre B, Jean DR (1986) Lack of the D2 protein in a Chlamydomonas reinhardtii psbD mutant affects Photosystem II stability and D1 expression. The EMBO Journal 5, 1745–1754.
Karaca M, Saha S, Callahan FE, Jenkins JN, Read JJ, Percy RG (2004) Molecular and cytological characterization of a cytoplasmic-specific mutant in pima cotton (Gossypium barbadense L.). Euphytica 139, 187–197.
| Molecular and cytological characterization of a cytoplasmic-specific mutant in pima cotton (Gossypium barbadense L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Kjtrk%3D&md5=3b36ac4990df725db5eaea207bf8608dCAS |
Komander D (2009) The emerging complexity of protein ubiquitination. Biochemical Society Transactions 37, 937–953.
| The emerging complexity of protein ubiquitination.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFGls7fM&md5=9168274c3f54b9ffee1126ffaa2ce123CAS |
Kumari R, Yadav G, Sharma V, Sharma V, Kumar S (2013) Cytosine hypomethylation at CHG and CHH sites in the pleiotropic mutants of Mendelian inheritance in Catharanthus roseus. Journal of Genetics 92, 499–511.
| Cytosine hypomethylation at CHG and CHH sites in the pleiotropic mutants of Mendelian inheritance in Catharanthus roseus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhs1yisLo%3D&md5=7c05218cbb7f4ae43cc18afe768175a0CAS |
Leelavathi S, Bhardwaj A, Kumar S, Dass A, Pathak R, Pandey SS, Tripathy BC, Padmalatha KV, Dhandapani G, Kanakachari M, Kumar PA, Cella R, Reddy V (2011) Genome-wide transcriptome and proteome analyses of tobacco psaA and psbA deletion mutants. Plant Molecular Biology 76, 407–423.
| Genome-wide transcriptome and proteome analyses of tobacco psaA and psbA deletion mutants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmslahtLw%3D&md5=abe7ae121e9fef9a8493206f97ee3de8CAS |
Li N, Zhang DS, Liu HS, Yin CS, Li XX, Liang WQ, Yuan Z, Xu B, Chu HW, Wang J (2006) The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. The Plant Cell 18, 2999–3014.
| The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXit1CltQ%3D%3D&md5=157e070fcc38515abcda854be74af286CAS |
Li RQ, Huang JZ, Zhao HJ, Fu HW, Li YF, Liu GZ, Shu QY (2014) A down-regulated epi-allele of the genomes uncoupled 4 gene generates a xantha marker trait in rice. Theoretical and Applied Genetics 127, 2491–2501.
| A down-regulated epi-allele of the genomes uncoupled 4 gene generates a xantha marker trait in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsFeksLrP&md5=b495c4437e574758de3e062e2d46fcebCAS |
Liu XG, Xu H, Zhang JY, Liang GW, Liu YT, Guo AG (2012) Effect of low temperature on chlorophyll biosynthesis in albinism line of wheat (Triticum aestivum L.) FA85. Plant Physiology 145, 384–394.
| Effect of low temperature on chlorophyll biosynthesis in albinism line of wheat (Triticum aestivum L.) FA85.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVOqsLfF&md5=7c58678c088db8582ee39f6c0032c82bCAS |
Liu YX, Liang X, Zhou FB, Zhang ZM (2017) Accessing the agronomic and photosynthesis-related traits of high-yielding winter wheat mutants induced by ultra-high pressure. Field Crops Research 213, 165–173.
| Accessing the agronomic and photosynthesis-related traits of high-yielding winter wheat mutants induced by ultra-high pressure.Crossref | GoogleScholarGoogle Scholar |
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression date using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.
| Analysis of relative gene expression date using real-time quantitative PCR and the 2−ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=7285049423f39fc741010fb6e065ac24CAS |
Marder JB, Chapman DJ, Telfer A, Nixon PJ, Barber J (1987) Identification of psbA and psbD gene products, D1 and D2, as reaction center proteins of photosystem II. Plant Molecular Biology 9, 325–333.
| Identification of psbA and psbD gene products, D1 and D2, as reaction center proteins of photosystem II.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXlvFGisLo%3D&md5=ba2f114e7ac0dd16e08537501a146883CAS |
Mirouze M, Paszkowski J (2011) Epigenetic contribution to stress adaptation in plants. Current Opinion in Plant Biology 14, 267–274.
| Epigenetic contribution to stress adaptation in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnt1KmsLw%3D&md5=d8dff373e7b1ce8d2b1b958b709fcf4aCAS |
Motohashi R, Ito T, Kobayashi M, Taji T, Nagata N, Asami T, Yoshida S, Yamaguchi-Shinozaki K, Shinozaki K (2003) Functional analysis of the 37 kDa inner envelope membrane polypeptide in chloroplast biogenesis using a Ds-tagged Arabidopsis pale-green mutant. The Plant Journal 34, 719–731.
| Functional analysis of the 37 kDa inner envelope membrane polypeptide in chloroplast biogenesis using a Ds-tagged Arabidopsis pale-green mutant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlsFels7k%3D&md5=897f4bc2834b6359ddc269664385c809CAS |
Muhammad A, Muhammad I, Harpinder RH, Dean S (2014) Wheat: the miracle cereal. In ‘Managing and breeding wheat for organic systems’. pp. 1–7. (Springer: Dordrecht, The Netherlands)
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research 8, 4321–4326.
| Rapid isolation of high molecular weight plant DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXmtVSmtL8%3D&md5=e5ac8040c9964b31b77c508d0d22b329CAS |
Nagashima A, Hanaoka M, Shikanai T, Fujiwara M, Kanamaru K, Takahashi H, Tanaka K (2004) The multiple-stress responsive plastid sigma factor, SIG5, directs activation of the psbD blue light-responsive promoter (BLRP) in Arabidopsis thaliana. Plant & Cell Physiology 45, 357–368.
| The multiple-stress responsive plastid sigma factor, SIG5, directs activation of the psbD blue light-responsive promoter (BLRP) in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjsFKhtL8%3D&md5=9a1f376dff75df3319d2b5996086be2aCAS |
Naydenov M, Baev V, Apostolova E, Gospodinova N, Sablok G, Gozmanova M, Yahubyan G (2015) High-temperature effect on genes engaged in DNA methylation and affected by DNA methylation in Arabidopsis. Plant Physiology and Biochemistry 87, 102–108.
| High-temperature effect on genes engaged in DNA methylation and affected by DNA methylation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXmtVSmuw%3D%3D&md5=66297ab93b3f709082e3a952e239a740CAS |
Portis E, Acquadro A, Comino C, Lanteri S (2004) Analysis of DNA methylation during germination of pepper (Capsicum annuum L.) seeds using methylation-sensitive amplification polymorphism (MSAP). Plant Science 166, 169–178.
| Analysis of DNA methylation during germination of pepper (Capsicum annuum L.) seeds using methylation-sensitive amplification polymorphism (MSAP).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltVyisg%3D%3D&md5=5739faf9ee277702b5aae1547a4da685CAS |
Qin DD, Dong J, Xu FC, Guo GG, Ge ST, Xu Q, Xu YX, Li MF (2015) Characterization and fine mapping of a novel barley stage green-revertible albino gene (Hv SGRA) by bulked segregant analysis based on SSR assay and specific length amplified fragment sequencing. BMC Genomics 16, 838
| Characterization and fine mapping of a novel barley stage green-revertible albino gene (Hv SGRA) by bulked segregant analysis based on SSR assay and specific length amplified fragment sequencing.Crossref | GoogleScholarGoogle Scholar |
Racolta A, Bryan AC, Tax FE (2014) The receptor-like kinases GSO1 and GSO2 together regulate root growth in Arabidopsis through control of cell division and cell fate specification. Developmental Dynamics 243, 257–278.
| The receptor-like kinases GSO1 and GSO2 together regulate root growth in Arabidopsis through control of cell division and cell fate specification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht1ehsbo%3D&md5=70ac086c272eeae245eed4f68b600f5aCAS |
Sawers RJH, Viney J, Farmer PR, Bussey RR, Olsefski G, Anufrikova K, Hunter CN, Brutnell TP (2006) The maize Oil yellow1 (Oy1) gene encodes the I subunit of magnesium chelatase. Plant Molecular Biology 60, 95–106.
| The maize Oil yellow1 (Oy1) gene encodes the I subunit of magnesium chelatase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFyntrY%3D&md5=cc1297ba28f3980ace8023fa49d76544CAS |
Shan XH, Wang XY, Yang G, Wu Y, Su SZ, Li SP, Liu HK, Yuan YP (2013) Analysis of the DNA methylation of maize (Zea mays L.) in response to cold stress based on methylation-sensitive amplified polymorphisms. Journal of Plant Biology 56, 32–38.
| Analysis of the DNA methylation of maize (Zea mays L.) in response to cold stress based on methylation-sensitive amplified polymorphisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXisVajurw%3D&md5=4653f484e75479b6ec3e10642a2cf2b2CAS |
Shen H, He H, Li J, Chen W, Wang X, Guo L, Peng Z, He G, Zhong S, Qi Y, Terzaghi W, Deng XW (2012) Genome-wide analysis of DNA methylation and gene expression changes in two Arabidopsis ecotypes and their reciprocal hybrids. The Plant Cell 24, 875–892.
| Genome-wide analysis of DNA methylation and gene expression changes in two Arabidopsis ecotypes and their reciprocal hybrids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xmsl2jtrs%3D&md5=4a310e60589e1756d533c3f16893beb3CAS |
Sheng Y, Zhang GS, Li YX, Zhang LY, Wang SP, Zhao XL, Wang LM, Song YL (2011) The relationship on anther tapetum, sporopollenin and expression of RAFTIN1 in physiological male sterile wheat. Scientia Agricultura Sinica 44, 3937–3944.
Slafer GA, Savin R, Sadras VO (2014) Coarse and fine regulation of wheat yield components in response to genotype and environment. Field Crops Research 157, 71–83.
| Coarse and fine regulation of wheat yield components in response to genotype and environment.Crossref | GoogleScholarGoogle Scholar |
Song YL, Wang JW, Zhang PF, Zhang GS, Zhang LY, Zhao XL, Niu N, Ma SC (2014) Cytochemical investigation at different microsporogenesis phases of male sterility in wheat, as induced by the chemical hybridising agent SQ. Crop & Pasture Science 65, 868–877.
| Cytochemical investigation at different microsporogenesis phases of male sterility in wheat, as induced by the chemical hybridising agent SQ.Crossref | GoogleScholarGoogle Scholar |
Sun Y, Wang X, Wang N, Chen Y, Zhang S (2014) Changes in the yield and associated photosynthetic traits of dry-land winter wheat (Triticum aestivum L.) from the 1940 to the 2010 in Shaanxi Province of China. Field Crops Research 167, 1–10.
| Changes in the yield and associated photosynthetic traits of dry-land winter wheat (Triticum aestivum L.) from the 1940 to the 2010 in Shaanxi Province of China.Crossref | GoogleScholarGoogle Scholar |
Vilperte V, Agapito-Tenfen SZ, Wikmark O-G, Nodari RO (2016) Levels of DNA methylation and transcript accumulation in leaves of transgenic maize varieties. Environmental Sciences Europe 28, 29
| Levels of DNA methylation and transcript accumulation in leaves of transgenic maize varieties.Crossref | GoogleScholarGoogle Scholar |
von Wettstein D, Simon G, Kannangara GC (1995) Chlorophyll biosynthesis. The Plant Cell 7, 1039–1057.
| Chlorophyll biosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnt1Sgt7o%3D&md5=97734b4947a33768eff61a7547f72fbdCAS |
Xu BQ, An MM, Jiang KY, Xu LL, Yang HY, Zhou MB (2015) Cloning and functional analysis of the psbD gene in Pseudosasa japonica f. Akebonosuji. Journal of Zhejiang A&F University 32, 557–565.
Xue Q, Soundararajan M, Weiss A, Arkebauer TJ, Baenziger PS (2002) Genotypic variation of gas exchange parameters and carbon isotope discrimination in winter wheat. Journal of Plant Physiology 159, 891–898.
| Genotypic variation of gas exchange parameters and carbon isotope discrimination in winter wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmvFOgurk%3D&md5=f5a564557416777209ba014d95c47141CAS |
Zeng G, Yu X, Cai M (2001) Regulation of yeast actin cytoskeleton-regulatory complex Pan1p/Sla1p/End3p by serine/threonine kinase Prk1p. Molecular Biology of the Cell 12, 3759–3772.
| Regulation of yeast actin cytoskeleton-regulatory complex Pan1p/Sla1p/End3p by serine/threonine kinase Prk1p.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXpt1Gitbo%3D&md5=55d2460d11547a819169d228c2339286CAS |
Zhao YL, Yu SX, Ye WW, Wang HM, Wang JJ, Fang BX (2010) Study on DNA cytosine methylation of cotton (Gossypium hirsutum L.) genome and its implication for salt tolerance. Agricultural Sciences in China 9, 783–791.
| Study on DNA cytosine methylation of cotton (Gossypium hirsutum L.) genome and its implication for salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpsVGku7Y%3D&md5=8cda6c482af5257788205ae376401e7cCAS |
Zhu XG, Long SP, Ort DR (2010) Improving photosynthetic efficiency for greater yield. Annual Review of Plant Biology 61, 235–261.
| Improving photosynthetic efficiency for greater yield.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnslSjsL8%3D&md5=8fd94bc0102d6d6a9f42f94a2a6f3471CAS |
