Promoter deletion analysis reveals root-specific expression of the alkenal reductase gene (OsAER1) in Oryza sativa
Aniversari Apriana A B , Atmitri Sisharmini B , Hajrial Aswidinnoor A , Kurniawan R. Trijatmiko B C and Sudarsono Sudarsono
A C
+ Author Affiliations
- Author Affiliations
A PMB Lab, Department of Agronomy and Horticulture, Faculty of Agriculture, Bogor Agricultural University, Jalan Raya Ciampea, Bogor, Indonesia.
B Indonesian Center for Agricultural Biotechnology and Genetic Resources Research and Development, Jalan Tentara Pelajar 3A, Bogor, Indonesia.
C Corresponding authors. Emails: s_sudarsono@ymail.com; krtrijatmiko@gmail.com
Functional Plant Biology 46(4) 376-391 https://doi.org/10.1071/FP18237
Submitted: 14 September 2018 Accepted: 12 January 2019 Published: 6 February 2019
Abstract
Root-specific promoters are useful in plant genetic engineering, primarily to improve water and nutrient absorption. The aim of this study was to clone and characterise the promoter of the Oryza sativa L. alkenal reductase (OsAER1) gene encoding 2-alkenal reductase, an NADPH-dependent oxidoreductase. Expression analysis using quantitative real-time PCR confirmed the root-specific expression of the OsAER1 gene. Subsequently, a 3082-bp fragment of the OsAER1 promoter was isolated from a local Indonesian rice cultivar, Awan Kuning. Sequencing and further nucleotide sequence analysis of the 3082-bp promoter fragment (PA-5) revealed the presence of at least 10 root-specific cis-regulatory elements putatively responsible for OsAER1 root-specific expression. Using the 3082-bp promoter fragment to drive the expression of the GUS reporter transgene confirmed that the OsAER1 promoter is root-specific. Further, the analysis indicated that OsAER1 promoter activity was absent in leaves, petioles and shoots during sprouting, vegetative, booting and generative stages of rice development. In contrast, the promoter activity was present in anthers and aleurone layers of immature seeds 7–20 days after anthesis. Moreover, there was no promoter activity observed in the aleurone layers of mature seeds. The OsAER1 promoter activity is induced by Al-toxicity, NaCl and submergence stresses, indicating the OsAER1 promoter activity is induced by those stresses. Exogenous treatments of transgenic plants carrying the PA-5 promoter construct with abscisic acid and indoleacetic acid also induced expression of the GUS reporter transgene, indicating the role of plant growth regulators in controlling OsAER1 promoter activity. Promoter deletion analysis was conducted to identify the cis-acting elements of the promoter responsible for controlling root-specific expression. The GUS reporter gene was fused with various deletion fragments of the OsAER1 promoter and the resulting constructs were transformed in rice plants to generate transgenic plants. The results of this analysis indicated that cis-acting elements controlling root-specific expression are located between −1562 to −1026 bp of the OsAER1 CDS. Here we discusses the results of the conducted analyses, the possible role of OsAER1 in rice growth and development, possible contributions and the potential usage of these findings in future plant research.
Additional keywords: cis-acting element, promoter deletion, root-specific expression, tissue-specific expression.
References
Agius F, Amaya I, Botella MA, Valpuesta V (2005) Functional analysis of homologous and heterologous promoters in strawberry fruits using transient expression. Journal of Experimental Botany 56, 37–46.Ahmad N, Mukhtar Z (2017) Genetic modifications of crop plants: issues and challenges. Genomics 109, 494–505.
| Genetic modifications of crop plants: issues and challenges.Crossref | GoogleScholarGoogle Scholar | 28778540PubMed |
Alemayehu D (2017) Application of genetic engineering in plant breeding for biotic stress resistance. International Journal of Research Studies in Biosciences 5, 28–35.
An-Qi G, Zhan-Jun Z, Xuan-Li N, Xing-Guo X (2009) Expression analysis of four-specific promoters of Brassica spp. in the heterogeneous host tobacco. African Journal of Biotechnology 8, 5193–5200.
Babiychuk E, Kushnir S, Belles-Boix E, Montagu MV, Inze D (1995) Arabidopsis thaliana NADPH oxidoreductase homologs confer tolerance of yeasts toward the thiol-oxidizing drug diamide. Journal of Biological Chemistry 270, 26224–26231.
| Arabidopsis thaliana NADPH oxidoreductase homologs confer tolerance of yeasts toward the thiol-oxidizing drug diamide.Crossref | GoogleScholarGoogle Scholar | 7592828PubMed |
Bakhsh A, Rao AQ, Shamim Z, Husnain T (2011) A mini review: rubisco small subunit as a strong, green tissue-specific promoter. Archives of Biological Sciences 63, 299–307.
| A mini review: rubisco small subunit as a strong, green tissue-specific promoter.Crossref | GoogleScholarGoogle Scholar |
Bhagat KP, Kumar RA, Ratnakumar P, Kumar S, Bal SK, Agrawal PK (2014) Photosynthesis and associated aspects under abiotic stresses environment. In ‘Approaches to plant stress and their management.’ (Eds RK Gaur, P Sharma) pp. 191–205. (Springer India: New Delhi)
Bishopp A, Bennett MJ (2014) Hormone crosstalk: directing the flow. Current Biology 24, R366–R368.
| Hormone crosstalk: directing the flow.Crossref | GoogleScholarGoogle Scholar | 24801187PubMed |
Biswas MS, Mano J (2015) Lipid peroxide-derived short-chain carbonyls mediate hydrogen peroxide-induced and salt-induced programmed cell death in plants. Plant Physiology 168, 885–898.
| Lipid peroxide-derived short-chain carbonyls mediate hydrogen peroxide-induced and salt-induced programmed cell death in plants.Crossref | GoogleScholarGoogle Scholar | 26025050PubMed |
Blazquez M (2007) Quantitative GUS activity assay of plant extracts. Cold Spring Harbor Protocols
| Quantitative GUS activity assay of plant extracts.Crossref | GoogleScholarGoogle Scholar | 21357025PubMed |
Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Annals of Botany 91, 179–194.
| Antioxidants, oxidative damage and oxygen deprivation stress: a review.Crossref | GoogleScholarGoogle Scholar | 12509339PubMed |
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
| A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 942051PubMed |
Carvalhais LC, Dennis PG, Fedoseyenko D, Hajirezaei M-R, Borriss R, von Wirén N (2011) Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency. Journal of Plant Nutrition and Soil Science 174, 3–11.
| Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency.Crossref | GoogleScholarGoogle Scholar |
Christ A, Maegele I, Ha N, Nguyen HH, Crespi MD, Maizel A (2013) In silico identification and in vivo validation of a set of evolutionary conserved plant root-specific cis-regulatory elements. Mechanisms of Development 130, 70–81.
| In silico identification and in vivo validation of a set of evolutionary conserved plant root-specific cis-regulatory elements.Crossref | GoogleScholarGoogle Scholar | 22504372PubMed |
Dar NA, Amin I, Wani W, Wani SA, Shikari AB, Wani SH, Masoodi KZ (2017) Abscisic acid: a key regulator of abiotic stress tolerance in plants. Plant Gene 11, 106–111.
| Abscisic acid: a key regulator of abiotic stress tolerance in plants.Crossref | GoogleScholarGoogle Scholar |
Deng ZY, Gong CY, Wang T (2013) Use of proteomics to understand seed development in rice. Proteomics 13, 1784–1800.
| Use of proteomics to understand seed development in rice.Crossref | GoogleScholarGoogle Scholar | 23483697PubMed |
Depuydt S, Hardtke CS (2011) Hormone signalling crosstalk in plant growth review regulation. Current Biology 21, R365–R373.
| Hormone signalling crosstalk in plant growth review regulation.Crossref | GoogleScholarGoogle Scholar | 21549959PubMed |
Escobar-Sepúlveda HF, Trejo-Telez LI, Garcoa-Morales S, Gomez-Merino FC (2017) Expression patterns and promoter analyses of aluminum-responsive NAC genes suggest a possible growth regulation of rice mediated by aluminum, hormones and NAC transcription factors. PLoS One 12, e0186084
| Expression patterns and promoter analyses of aluminum-responsive NAC genes suggest a possible growth regulation of rice mediated by aluminum, hormones and NAC transcription factors.Crossref | GoogleScholarGoogle Scholar | 29023561PubMed |
Fehlberg V, Vieweg MF, Dohmann EM, Hohnjec N, Puhler A, Perlick AM, Kuster H (2005) The promoter of the leghaemoglobin gene VfLb29: functional analysis and identification of modules necessary for its activation in the infected cells of root nodules and in the arbuscule-containing cells of mycorrhizal roots. Journal of Experimental Botany 56, 799–806.
| The promoter of the leghaemoglobin gene VfLb29: functional analysis and identification of modules necessary for its activation in the infected cells of root nodules and in the arbuscule-containing cells of mycorrhizal roots.Crossref | GoogleScholarGoogle Scholar | 15668224PubMed |
Ghanem ME, Hichri I, Smigocki AC, Albacete A, Fauconnier ML, Diatloff E, Martinez-Andujar C, Lutts S, Dodd IC, Pérez-Alfocea F (2011) Root-targeted biotechnology to mediate hormonal signalling and improve crop stress tolerance. Plant Cell Reports 30, 807–823.
| Root-targeted biotechnology to mediate hormonal signalling and improve crop stress tolerance.Crossref | GoogleScholarGoogle Scholar | 21298270PubMed |
Gregorio GB, Senadhira D, Mendoza RD, Manigbas NL, Roxas JP, Guerta CQ (2002) Progress in breeding for salinity tolerance and associated abiotic stresses in rice. Field Crops Research 76, 91–101.
| Progress in breeding for salinity tolerance and associated abiotic stresses in rice.Crossref | GoogleScholarGoogle Scholar |
Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Molecular Biology 49, 373–385.
| Auxin-responsive gene expression: genes, promoters and regulatory factors.Crossref | GoogleScholarGoogle Scholar | 12036261PubMed |
Hernandez-Garcia CM, Finer JJ (2014) Identification and validation of promoters and cis-acting regulatory elements. Plant Science 217–218, 109–119.
| Identification and validation of promoters and cis-acting regulatory elements.Crossref | GoogleScholarGoogle Scholar | 24467902PubMed |
Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Research 27, 297–300.
| Plant cis-acting regulatory DNA elements (PLACE) database: 1999.Crossref | GoogleScholarGoogle Scholar | 9847208PubMed |
Hirata T, Tamura Y, Yokobatake N, Shimoda K, Ashida Y (2000) A 38 kDa allylic alcohol dehydrogenase from the cultured cells of Nicotiana tabacum. Phytochemistry 55, 297–303.
| A 38 kDa allylic alcohol dehydrogenase from the cultured cells of Nicotiana tabacum.Crossref | GoogleScholarGoogle Scholar | 11117876PubMed |
Hobo T, Suwabe K, Aya K, Suzuki G, Yano K, Ishimizu T, Fujita M, Kikuchi S, Hamada K, Miyano M, et al (2008) Various spatiotemporal expression profiles of anther-expressed genes in rice. Plant and Cell Physiology 49, 1417–1428.
| Various spatiotemporal expression profiles of anther-expressed genes in rice.Crossref | GoogleScholarGoogle Scholar | 18776202PubMed |
Hoekema A, Hirsch PR, Hooykaas PJJ, Schilperoort RA (1983) A binary plant vector strategy based on separation of vir- and T-region of the Agrobacterium tumefaciens Ti-plasmid. Nature 303, 179–180.
| A binary plant vector strategy based on separation of vir- and T-region of the Agrobacterium tumefaciens Ti-plasmid.Crossref | GoogleScholarGoogle Scholar |
Holsters M, de Waele D, Depicker A, Messens E, van Montagu M, Schell J (1978) Transfection and transformation of Agrobacterium tumefaciens. Molecular & General Genetics 163, 181–187.
| Transfection and transformation of Agrobacterium tumefaciens.Crossref | GoogleScholarGoogle Scholar |
Inukai Y, Sakamoto T, Ueguchi-Tanaka M, Shibata Y, Gomi K, Umemura I, Hasegawa Y, Ashikari M, Kitano H, Matsuoka M (2005) Crown rootless1, which is essential for crown root formation in rice, is a target of an AUXIN RESPONSE FACTOR in auxin signaling. The Plant Cell 17, 1387–1396.
| Crown rootless1, which is essential for crown root formation in rice, is a target of an AUXIN RESPONSE FACTOR in auxin signaling.Crossref | GoogleScholarGoogle Scholar | 15829602PubMed |
Islam MM, Ye W, Matsushima D, Munemasa S, Nakamura Y, Biswas S, Mano J, Okuma E, Murata Y (2016) Reactive carbonyl species mediate ABA signaling in guard cells. Plant & Cell Physiology 57, 2552–2563.
| Reactive carbonyl species mediate ABA signaling in guard cells.Crossref | GoogleScholarGoogle Scholar |
Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO Journal 6, 3901–3907.
| GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants.Crossref | GoogleScholarGoogle Scholar | 3327686PubMed |
Jeong HJ, Jung KH (2015) Rice tissue-specific promoters and condition-dependent promoters for effective translational application. Journal of Integrative Plant Biology 57, 913–924.
| Rice tissue-specific promoters and condition-dependent promoters for effective translational application.Crossref | GoogleScholarGoogle Scholar | 25882130PubMed |
Jeong JS, Kim YS, Baek KH, Jung H, Ha S-H (2010) Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought condition. Plant Physiology 153, 185–197.
| Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought condition.Crossref | GoogleScholarGoogle Scholar | 20335401PubMed |
Jiang H-X, Yang L-T, Qi Y-P, Lu Y-B, Huang Z-R, Chen L-S (2015) Root iTRAQ protein profile analysis of two Citrus species differing in aluminium-tolerance in response to long-term aluminum-toxicity. BMC Genomics 16, 949
| Root iTRAQ protein profile analysis of two Citrus species differing in aluminium-tolerance in response to long-term aluminum-toxicity.Crossref | GoogleScholarGoogle Scholar | 26573913PubMed |
Jiao Y, Ma L, Strickland E, Denga XW (2005) Conservation and divergence of light-regulated genome expression patterns during seedling development in rice and Arabidopsis. The Plant Cell 17, 3239–3256.
| Conservation and divergence of light-regulated genome expression patterns during seedling development in rice and Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 16284311PubMed |
Jones MO, Maning K, Andrews J, Wright C, Taylor IB, Thompson AJ (2008) The promoter from SlREO, a highly-expressed, root-specific Solanum lycopersicum gene, directs expression to cortex of mature roots. Functional Plant Biology 35, 1224–1233.
| The promoter from SlREO, a highly-expressed, root-specific Solanum lycopersicum gene, directs expression to cortex of mature roots.Crossref | GoogleScholarGoogle Scholar |
Kagaya Y, Ohmiya K, Hattori T (1999) RAV1, a novel DNA-binding protein, binds to bipartite recognition sequence through two distinct DNA-binding domains uniquely found in higher plants. Nucleic Acids Research 27, 470–478.
| RAV1, a novel DNA-binding protein, binds to bipartite recognition sequence through two distinct DNA-binding domains uniquely found in higher plants.Crossref | GoogleScholarGoogle Scholar | 9862967PubMed |
Karuppanapandian T, Rhee S-J, Kim E-J, Han BK, Hoekenga OA, Lee GP (2012) Proteomic analysis of differentially expressed proteins in the roots of Columbia-0 and Landsberg erecta ecotypes of Arabidopsis thaliana in response to aluminum toxicity. Canadian Journal of Plant Science 92, 1267–1282.
| Proteomic analysis of differentially expressed proteins in the roots of Columbia-0 and Landsberg erecta ecotypes of Arabidopsis thaliana in response to aluminum toxicity.Crossref | GoogleScholarGoogle Scholar |
Kato-Noguchi H (2000) Abscisic acid and hypoxic induction of anoxia tolerance in roots of lettuce seedlings. Journal of Experimental Botany 51, 1939–1944.
| Abscisic acid and hypoxic induction of anoxia tolerance in roots of lettuce seedlings.Crossref | GoogleScholarGoogle Scholar | 11113172PubMed |
Kim K-N, Guiltinan MJ (1999) Identification of cis-acting elements important for expression of the starch-branching enzyme I gene in maize endosperm. Plant Physiology 121, 225–236.
| Identification of cis-acting elements important for expression of the starch-branching enzyme I gene in maize endosperm.Crossref | GoogleScholarGoogle Scholar | 10482678PubMed |
Kim DW, Lee SH, Choi S-B, Won S-K, Heo Y-K, Cho M, Park YI, Choa HT (2006) Functional conservation of a root hair cell-specific cis-element in angiosperms with different root hair distribution patterns. The Plant Cell 18, 2958–2970.
| Functional conservation of a root hair cell-specific cis-element in angiosperms with different root hair distribution patterns.Crossref | GoogleScholarGoogle Scholar | 17098810PubMed |
Klinedinst S, Pascuzzi P, Redman J, Desai M, Arias J (2000) A xenobiotic-stress-activated transcription factor and its cognate target genes are preferentially expressed in root tip meristems. Plant Molecular Biology 42, 679–688.
| A xenobiotic-stress-activated transcription factor and its cognate target genes are preferentially expressed in root tip meristems.Crossref | GoogleScholarGoogle Scholar | 10809441PubMed |
Koyro H-W, Ahmad P, Geissler N (2012) Abiotic stress responses in plants: an overview. In ‘Environmental adaptations and stress tolerance of plants in the era of climate change’. (Eds P Ahmad and MNV Prasad) pp. 1–28. (Springer: NY)
Li M, Singh R, Bazanova N, Milligan AS, Shirley N, Langridge P, Lopato S (2008) Spatial and temporal expression of endosperm transfer cell-specific promoters in transgenic rice and barley. Plant Biotechnology Journal 6, 465–476.
| Spatial and temporal expression of endosperm transfer cell-specific promoters in transgenic rice and barley.Crossref | GoogleScholarGoogle Scholar | 18422887PubMed |
Li Y, Liu S, Yu Z, Liu Y, Wu P (2013) Isolation and characterization of two novel root-specific promoters in rice (Oryza sativa L.). Plant Science 207, 37–44.
| Isolation and characterization of two novel root-specific promoters in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 23602097PubMed |
Makhloufi E, Yousfi Mi F-E, Marande W, Mila I, Hanana M, Berges H, Mzid R, Bouzayen M (2014) Isolation and molecular characterization of EFR1, an ethylene response factor gene from durum wheat (Triticum turgidum L. subsp. durum), potentially involved in salt-stress responses. Journal of Experimental Botany 65, 6359–6371.
| Isolation and molecular characterization of EFR1, an ethylene response factor gene from durum wheat (Triticum turgidum L. subsp. durum), potentially involved in salt-stress responses.Crossref | GoogleScholarGoogle Scholar | 25205575PubMed |
Mano J, Belles-Boix E, Babiychuk E, Inze D, Torii Y, Hiraoka E, Takimoto K, Slooten L, Asada K, Kushnir S (2005) Protection against photooxidative injury of tobacco leaves by 2 alkenal reductase detoxication of lipid peroxide-derived reactive carbonyls. Plant Physiology 139, 1773–1783.
| Protection against photooxidative injury of tobacco leaves by 2 alkenal reductase detoxication of lipid peroxide-derived reactive carbonyls.Crossref | GoogleScholarGoogle Scholar | 16299173PubMed |
Masuda H, Ishimaru Y, Aung MS, Kobayashi T, Kakei Y, Takahashi M, Higuchi K, Nakanishi H, Nishizawa NK (2012) Iron biofortification in rice by the introduction of multiple genes involved in iron nutrition. Scientific Reports 2, 543
| Iron biofortification in rice by the introduction of multiple genes involved in iron nutrition.Crossref | GoogleScholarGoogle Scholar | 22848789PubMed |
Mohanty B, Krishnan SPT, Swarup S, Bajic VB (2005) Detection and preliminary analysis of motifs in promoters of anaerobically induced genes of different plant species. Annals of Botany 96, 669–681.
| Detection and preliminary analysis of motifs in promoters of anaerobically induced genes of different plant species.Crossref | GoogleScholarGoogle Scholar | 16027132PubMed |
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassay with tobacco tissue cultures. Physiologia Plantarum 15, 473–497.
| A revised medium for rapid growth and bioassay with tobacco tissue cultures.Crossref | GoogleScholarGoogle Scholar |
Nitz I, Berkefeld H, Puzio PS, Grundler FMW (2001) Pyk10, a seedling and root-specific gene and promoter from Arabidopsis thaliana. Plant Science 161, 337–346.
| Pyk10, a seedling and root-specific gene and promoter from Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 11448764PubMed |
Panda SK, Baluska F, Matsumoto H (2009) Aluminum stress signaling in plants. Plant Signaling & Behavior 4, 592–597.
| Aluminum stress signaling in plants.Crossref | GoogleScholarGoogle Scholar |
Parmar N, Singh KH, Sharma D, Singh L, Kumar P, Nanjundan J, Khan YJ, Chauhan DK, Thakur K (2017) Genetic engineering strategies for biotic and abiotic stress tolerance and quality enhancement in horticultural crops: a comprehensive review. 3 Biotech 7, 239–274.
| Genetic engineering strategies for biotic and abiotic stress tolerance and quality enhancement in horticultural crops: a comprehensive review.Crossref | GoogleScholarGoogle Scholar | 28702937PubMed |
Prestridge DS (1991) SIGNAL SCAN: a computer program that scans DNA sequences for eukaryotic transcriptional elements. Computer Applications in the Biosciences 7, 203–206.
Redman J, Whitcraft J, Johnson C, Arias J (2002) Abiotic and biotic stress differentially stimulate as-1 element activity in Arabidopsis. Plant Cell Reports 21, 180–185.
| Abiotic and biotic stress differentially stimulate as-1 element activity in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Reddy INBL, Kim B-K, Yoon I-S, Kim K-H, Kwon T-R (2017) Salt tolerance in rice: focus on mechanisms and approaches. Rice Science 24, 123–144.
| Salt tolerance in rice: focus on mechanisms and approaches.Crossref | GoogleScholarGoogle Scholar |
Ryan PR, Delhaize E, Watt M, Richardson AE (2016) Preface: part of a special issue on root biology. Plant roots: understanding structure and function in an ocean of complexity. Annals of Botany 118, 555–559.
| Preface: part of a special issue on root biology. Plant roots: understanding structure and function in an ocean of complexity.Crossref | GoogleScholarGoogle Scholar |
Sadimantara GR, Muhidin M, Leomo S (2014) Tolerance test of some progenies of local upland rice (Oryza sativa L.) crosses against aluminum stress. Australian Journal of Basic and Applied Sciences 8, 1–6.
Selvaraj MG, Ogawa S, Lu Y, Wu L, Down C, Skinner W, Lu Z, Kridl JC, Ishitani M, van Boxtel J (2017) Development and field performance of nitrogen use efficient rice lines for Africa. Plant Biotechnology Journal 15, 775–787.
| Development and field performance of nitrogen use efficient rice lines for Africa.Crossref | GoogleScholarGoogle Scholar | 27889933PubMed |
Sharma N, Russell SD, Bhalla PL, Singh MB (2011) Putative cis-regulatory elements in genes highly expressed in rice sperm cells. BMC Research Notes 4, 319
| Putative cis-regulatory elements in genes highly expressed in rice sperm cells.Crossref | GoogleScholarGoogle Scholar | 21892935PubMed |
Shrawat AK, Carroll RT, DePauw M, Taylor GJ, Good GA (2008) Genetic engineering of improved nitrogen use efficiency in rice by the tissue-specific expression of alanine aminotransferase. Plant Biotechnology Journal 6, 722–732.
| Genetic engineering of improved nitrogen use efficiency in rice by the tissue-specific expression of alanine aminotransferase.Crossref | GoogleScholarGoogle Scholar | 18510577PubMed |
Slamet-Loedin IH, Chadha-Mohanty P, Torrizo L (2014) Agrobacterium-mediated transformation: rice transformation. In ‘Methods in molecular biology. Cereal genomics methods and protocols’. (Eds RJ Henry, A Furtado) pp. 261–272. (Springer: NY)
Song P, Heinen JL, Burns TH, Allen RD (2000) Expression of two tissue-specific promoters in transgenic cotton plants. Journal of Cotton Science 4, 217–223.
Sun P, Tian Q-Y, Chen J, Zhang W-H (2010) Aluminum-induced inhibition of root elongation in Arabidopsis is mediated by ethylene and auxin. Journal of Experimental Botany 61, 347–356.
| Aluminum-induced inhibition of root elongation in Arabidopsis is mediated by ethylene and auxin.Crossref | GoogleScholarGoogle Scholar | 19858117PubMed |
Trachsel S, Stamp P, Hund A (2010) Effect of high temperatures, drought and aluminum toxicity on root growth of tropical maize (Zea mays L.) seedlings. Maydica 55, 249–260.
Trijatmiko KR, Dueñas C, Tsakirpaloglou N, Torrizo L, Arines FM, Adeva C, Balindong J, Oliva N, Sapasap MV, Borrero J, et al (2016) Biofortified indica rice attains iron and zinc nutrition dietary targets in the field. Scientific Reports 6, 19792
| Biofortified indica rice attains iron and zinc nutrition dietary targets in the field.Crossref | GoogleScholarGoogle Scholar | 26806528PubMed |
Unni SC, Vivek PJ, Maju TT, Varghese RT, Soniya EV (2012) Molecular cloning and characterization of fruit-specific promoter from Cucumis sativus L. American Journal of Molecular Biology 2, 132–139.
| Molecular cloning and characterization of fruit-specific promoter from Cucumis sativus L.Crossref | GoogleScholarGoogle Scholar |
Upreti KK, Sharma M (2016) Role of plant growth regulators in abiotic stress tolerance, In ‘Abiotic stress physiology of horticultural crops’. (Eds NKS Rao, KS Shivashankara, RH Laxman) pp. 19–46. (Springer India: New Delhi)
Varnier A-L, Mazeyrat-Gourbeyre F, Sangwan RS, Clement C (2005) Programmed cell death progressively models the development of anther sporophytic tissues from the tapetum and is triggered in pollen grains during maturation. Journal of Structural Biology 152, 118–128.
| Programmed cell death progressively models the development of anther sporophytic tissues from the tapetum and is triggered in pollen grains during maturation.Crossref | GoogleScholarGoogle Scholar | 16256370PubMed |
Wang R-S, Pandey S, Li S, Gookin TE, Zhao Z, Albert A, Assmann SM (2011) Common and unique elements of the ABA-regulated transcriptome of Arabidopsis guard cells. BMC Genomics 12, 216
| Common and unique elements of the ABA-regulated transcriptome of Arabidopsis guard cells.Crossref | GoogleScholarGoogle Scholar | 21554708PubMed |
Wang T, Li C, Wu Z, Jia Y, Wang H, Sun S, Mao C, Wang X (2017) Abscisic acid regulates auxin homeostasis in rice root tips to promote root hair elongation. Frontiers of Plant Science 8, 1121
| Abscisic acid regulates auxin homeostasis in rice root tips to promote root hair elongation.Crossref | GoogleScholarGoogle Scholar |
Warren JM, Hanson PJ, Iversen CM, Kumar J, Walker AP, Wullschleger SD (2015) Root structural and functional dynamics in terrestrial biosphere models – evaluation and recommendations. New Phytologist 205, 59–78.
| Root structural and functional dynamics in terrestrial biosphere models – evaluation and recommendations.Crossref | GoogleScholarGoogle Scholar | 25263989PubMed |
Wei L, Wang L, Yang Y, Wang P, Guo T, Kang G (2015) Abscisic acid enhances tolerance of wheat seedlings to drought and regulates transcript levels of genes encoding ascorbate-glutathione biosynthesis. Frontiers of Plant Science 6, 458
| Abscisic acid enhances tolerance of wheat seedlings to drought and regulates transcript levels of genes encoding ascorbate-glutathione biosynthesis.Crossref | GoogleScholarGoogle Scholar |
Wen C-L, Cheng Q, Zhao L, Mao A, Yang J, Yu S, Weng Y, Xu Y (2016) Identification and characterization of Dof transcription factors in the cucumber genome. Scientific Reports 6, 23072
| Identification and characterization of Dof transcription factors in the cucumber genome.Crossref | GoogleScholarGoogle Scholar | 26979661PubMed |
Wijerathna-Yapa A (2017) Transgenic plants: resistance to abiotic and biotic stresses. Journal of Agriculture and Environment for International Development 111, 245–275.
Wu W, Cheng S (2014) Root genetic research, an opportunity and challenge to rice improvement. Field Crops Research 165, 111–124.
| Root genetic research, an opportunity and challenge to rice improvement.Crossref | GoogleScholarGoogle Scholar |
Wu Y, Cai Y, Sun Y, Xu R, Yu H, Han X, Lou H, Cheng A (2013) A single amino acid determines the catalytic efficiency of two alkenal double bond reductases produced by the liverwort Plagiochasma appendiculatum. FEBS Letters 587, 3122–3128.
| A single amino acid determines the catalytic efficiency of two alkenal double bond reductases produced by the liverwort Plagiochasma appendiculatum.Crossref | GoogleScholarGoogle Scholar | 23954295PubMed |
Wu Y-F, Zheng H-B, Liu X-Y, Cheng A-X, Lou H-Y (2018) Molecular diversity of alkenal double bond reductases in the liverwort Marchantia paleacea. Molecules 23, 1630
| Molecular diversity of alkenal double bond reductases in the liverwort Marchantia paleacea.Crossref | GoogleScholarGoogle Scholar |
Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends in Plant Science 10, 88–94.
| Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters.Crossref | GoogleScholarGoogle Scholar | 15708346PubMed |
Yamamoto YT, Taylor CG, Acedo GN, Cheng C-L, Conkling MA (1991) Characterization of cis-acting sequences regulating root-specific gene expression in tobacco. The Plant Cell 3, 371–382.
| Characterization of cis-acting sequences regulating root-specific gene expression in tobacco.Crossref | GoogleScholarGoogle Scholar | 1840917PubMed |
Yamauchi Y, Hasegawa A, Taninaka A, Mizutani M, Sugimoto Y (2011) NADPH-dependent reductases involved in the detoxification of reactive carbonyls in plants. Journal of Biological Chemistry 286, 6999–7009.
| NADPH-dependent reductases involved in the detoxification of reactive carbonyls in plants.Crossref | GoogleScholarGoogle Scholar | 21169366PubMed |
Yamauchi Y, Hasegawa A, Mizutani M, Sugimoto Y (2012) Chloroplastic NADPH dependent alkenal/one oxidoreductase contributes to the detoxification of reactive carbonyls produced under oxidative stress. FEBS Letters 586, 1208–1213.
| Chloroplastic NADPH dependent alkenal/one oxidoreductase contributes to the detoxification of reactive carbonyls produced under oxidative stress.Crossref | GoogleScholarGoogle Scholar | 22575657PubMed |
Yan D, Duermeyer L, Leoveanu C, Nambara E (2014) The functions of the endosperm during seed germination. Plant & Cell Physiology 55, 1521–1533.
| The functions of the endosperm during seed germination.Crossref | GoogleScholarGoogle Scholar |
Yang Z-B, Rao IM, Horst WEJ (2013) Interaction of aluminum and drought stress on root growth and crop yield on acid soils. Plant and Soil 372, 3–25.
| Interaction of aluminum and drought stress on root growth and crop yield on acid soils.Crossref | GoogleScholarGoogle Scholar |
Yin L, Mano J, Wang S, Tsuji W, Tanaka K (2010) The involvement of lipid peroxide-derived aldehydes in aluminum toxicity of tobacco roots. Plant Physiology 152, 1406–1417.
| The involvement of lipid peroxide-derived aldehydes in aluminum toxicity of tobacco roots.Crossref | GoogleScholarGoogle Scholar | 20023145PubMed |
Zhang D-S, Liang W-Q, Yuan Z, Li N, Shi J, Wang J, Liu Y-M, Yu W-J, Zhang D-B (2008) Tapetum degeneration retardation is critical for aliphatic metabolism and gene regulation during rice pollen development. Molecular Plant 1, 599–610.
| Tapetum degeneration retardation is critical for aliphatic metabolism and gene regulation during rice pollen development.Crossref | GoogleScholarGoogle Scholar | 19825565PubMed |
Zhou S-R, Yin L-L, Xue H-W (2013) Functional genomics based understanding of rice endosperm development. Current Opinion in Plant Biology 16, 236–246.
| Functional genomics based understanding of rice endosperm development.Crossref | GoogleScholarGoogle Scholar | 23582455PubMed |
Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167, 313–324.
| Abiotic stress signaling and responses in plants.Crossref | GoogleScholarGoogle Scholar | 27716505PubMed |
