The seed-borne Southern bean mosaic virus hinders the early events of nodulation and growth in Rhizobium-inoculated Phaseolus vulgaris L.
Mariadaniela López A , Nacira Muñoz B C , Hernan Ramiro Lascano B C and María Luisa Izaguirre-Mayoral D E
+ Author Affiliations
- Author Affiliations
A Universidad Centroccidental Lisandro Alvarado, Postgrado de Agronomia, Laboratorio de Virologia, Barquisimeto 03023, Venezuela.
B Instituto de Fisiología y Recursos Genéticos Vegetales, Centro de Investigaciones Agropecuarias – Instituto Nacional de Tecnología Agropecuaria, 5119 Córdoba, Argentina.
C Cátedra de Fisiología Vegetal, Facultad de Ciencias Exactas Físicas y Naturales, Universidad Nacional de Córdoba, Avenida Vélez Sársfield 1611 Córdoba, Argentina.
D Instituto Venezolano de Investigaciones Científicas, Centro de Microbiología y Biología Celular, apartado postal 21827 Caracas 1020-A, Venezuela.
E Corresponding author. Email: mlizaguirre@gmail.com
Functional Plant Biology 44(2) 208-218 https://doi.org/10.1071/FP16180
Submitted: 12 May 2016 Accepted: 6 September 2016 Published: 20 October 2016
Abstract
To simulate seed-borne virus transmission, a noninvasive protocol was designed to infect the radicle of germinating seeds, with 100% effectiveness. Preinfection of 24-h-old black bean (Phaseolus vulgaris L.) radicles by Southern bean mosaic virus (SBMV) followed by Rhizobium inoculation 48 h later caused a drastic reduction in root nodulation. Results were attributed to active virus replication within the elongating zone of the radicle at least 32 h before Rhizobium inoculation, which elicited severe anatomical malformations; an abnormal accumulation of apoplastic reactive oxygen species in the rhizodermis, cortex, inner cortical and endodermic root cells; the formation of atypical root hair tips and the collapse of 94% of the root hairs in the SBMV-preinfected radicles. Adult SBMV-preinfected plants showed exacerbated virus symptoms and 80% growth reduction ascribed to major virus-induced ultrastructural alterations in the nodules. The accumulation of ureides, α−amino acids and total reducing sugars in the leaves and nodules of SBMV-preinfected plants are indicators of the hindering effects of SBMV infection on N2 fixation and ureide catabolism, causing N starvation. The exogenous addition of 1 or 4 μM naringenin, genistein or daidzein did not counteract the deleterious effects of SBMV preinfection on nodulation.
Additional keywords: amino acids, nodule ultrastructure, reactive oxygen species, root hairs, total reducing sugars, ureides.
References
Al-Shahwan IM, Abdalla OA, Al-Saleh MA, Am MA (2016) Detection of new viruses in alfalfa, weeds and cultivated plants growing adjacent to alfalfa fields in Saudi Arabia. Saudi Journal of Biological Sciences| Detection of new viruses in alfalfa, weeds and cultivated plants growing adjacent to alfalfa fields in Saudi Arabia.Crossref | GoogleScholarGoogle Scholar |
Alazem M, Lin NS (2015) Roles of plant hormones in the regulation of host–virus interactions. Molecular Plant Pathology 16, 529–540.
| Roles of plant hormones in the regulation of host–virus interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXotVektLY%3D&md5=c5fbe6ba7e331c2e4f64cf65d1261845CAS | 25220680PubMed |
Aparicio F, Pallás V (2016) The coat protein of Alfalfa mosaic virus interacts and interferes with the transcriptional activity of the bHLH transcription factor ILR3 promoting salicylic‐dependent defense signaling response. Molecular Plant Pathology
| The coat protein of Alfalfa mosaic virus interacts and interferes with the transcriptional activity of the bHLH transcription factor ILR3 promoting salicylic‐dependent defense signaling response.Crossref | GoogleScholarGoogle Scholar | 26929142PubMed |
Ball EM, Hampton RO, De Boer SH, Schaad NW (1993) Polyclonal antibodies. In ‘Serological methods for detection and identification of viral and bacterial plant pathogens. A laboratory manual’. (Eds R Hampton, E Ball, S De Boer) pp. 47–48. (APS Press: St Paul, MN)
Baral B, Teixeira da Silva JA, Izaguirre-Mayoral ML (2016) Early signaling, synthesis, transport and metabolism of ureides. Journal of Plant Physiology 193, 97–109.
| Early signaling, synthesis, transport and metabolism of ureides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XivVClt7Y%3D&md5=0ecb9ba62ab763681b3610c2ee5f1b9fCAS | 26967003PubMed |
Botelho SRA, Martins TP, Duarte MF, Barbosa AV, Lau D, Fernandes FR, Sanches MM (2016) Development of methodologies for virus detection in soybean and wheat seeds. MethodsX 3, 62–68.
| Development of methodologies for virus detection in soybean and wheat seeds.Crossref | GoogleScholarGoogle Scholar |
Congdon BS, Coutts BA, Renton M, Jones R (2016) Pea seed-borne mosaic virus: stability and wind-mediated contact transmission in field pea. Plant Disease 100, 953–958.
| Pea seed-borne mosaic virus: stability and wind-mediated contact transmission in field pea.Crossref | GoogleScholarGoogle Scholar |
Coutts BA, Prince RT, Jones RAC (2009) Quantifying effects of seedborne inoculum on virus spread, yield losses, and seed infection in the Pea seed-borne mosaic virus–field pea pathosystem. Phytopathology 99, 1156–1167.
| Quantifying effects of seedborne inoculum on virus spread, yield losses, and seed infection in the Pea seed-borne mosaic virus–field pea pathosystem.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1Mnht1ygsQ%3D%3D&md5=121c1960eb476d064224ddbaabfae42dCAS | 19740029PubMed |
Dakora FD, Joseph CM, Phillips DA (1993) Common bean root exudates contain elevated levels of diadzein and coumestrol in response to Rhizobium inoculation. Molecular Plant—Microbe Interactions 6, 665–668.
| Common bean root exudates contain elevated levels of diadzein and coumestrol in response to Rhizobium inoculation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXitFamtbs%3D&md5=c83edc97086692104ae644a2d4c99ae3CAS |
Datta S, Kim CM, Pernas M, Pires ND, Proust H, Tam T, Vijayakumar P, Dolan L (2011) Root hairs: development, growth and evolution at the plant–soil interface. Plant and Soil 346, 1–14.
| Root hairs: development, growth and evolution at the plant–soil interface.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtValtbvI&md5=dd62957e7cb6a6e1369602a83bbf486cCAS |
Fernández de Castro I, Tenorio R, Risco C (2016) Virus assembly factories in a lipid world. Current Opinion in Virology 18, 20–26.
| Virus assembly factories in a lipid world.Crossref | GoogleScholarGoogle Scholar | 26985879PubMed |
de Souza EM, Granada CE, Sperotto RA (2016) Plant pathogens affecting the establishment of plant–symbiont interaction. Frontiers in Plant Science 7, 15
| Plant pathogens affecting the establishment of plant–symbiont interaction.Crossref | GoogleScholarGoogle Scholar | 26834779PubMed |
Demidchik V (2015) Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. Environmental and Experimental Botany 109, 212–228.
| Mechanisms of oxidative stress in plants: from classical chemistry to cell biology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlaiur%2FM&md5=2acba29562dc1d7e2248080d29296fffCAS |
Domier LL, Hobbs HA, McCoppin NK, Bowen CR, Steinlage TA, Chang A, Wang Y, Hartman GL (2011) Multiple loci condition seed transmission of Soybean mosaic virus (SMV) and SMV-induced seed coat mottling in soybean. Phytopathology 101, 750–756.
| Multiple loci condition seed transmission of Soybean mosaic virus (SMV) and SMV-induced seed coat mottling in soybean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvFOmsb8%3D&md5=86450cdf4bd351d1dc41cfa88b2e426dCAS | 21561316PubMed |
Fiallo-Olivé E, Márquez-Martín B, Hassan I, Chirinos DT, Geraud-Pouey F, Navas-Castillo J, Moriones E (2013) Complete genome sequences of two novel begomoviruses infecting common bean in Venezuela. Archives of Virology 158, 723–727.
| Complete genome sequences of two novel begomoviruses infecting common bean in Venezuela.Crossref | GoogleScholarGoogle Scholar | 23178970PubMed |
Gautam NK, Kumar K, Prasad M (2016) Leaf crinkle disease in urdbean (Vigna mungo L. Hepper): an overview on causal agent, vector and host. Protoplasma 253, 729–746.
| Leaf crinkle disease in urdbean (Vigna mungo L. Hepper): an overview on causal agent, vector and host.Crossref | GoogleScholarGoogle Scholar | 26779639PubMed |
Giakountis A, Skoufa A, Paplomatas EI, Tokatlidis IS, Chatzivassiliou EK (2015) Molecular characterization and phylogenetic analysis of a Greek lentil isolate of Pea seed-borne mosaic virus. Phytoparasitica 43, 615–628.
| Molecular characterization and phylogenetic analysis of a Greek lentil isolate of Pea seed-borne mosaic virus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhslOgt7fP&md5=557152a1c3c8d97e9cf23b24a52b6a08CAS |
Grierson C, Nielsen E, Ketelaarc T, Schiefelbein J (2014) Root hairs. The Arabidopsis Book 12, e0172
| Root hairs.Crossref | GoogleScholarGoogle Scholar | 24982600PubMed |
Groves C, German T, Dasgupta R, Mueller D, Smith DL (2016) Seed transmission of Soybean vein necrosis virus: the first Tospovirus implicated in seed transmission. PLoS One 11, e0147342
| Seed transmission of Soybean vein necrosis virus: the first Tospovirus implicated in seed transmission.Crossref | GoogleScholarGoogle Scholar | 26784931PubMed |
Ibdah M, Dubey NK, Eizenberg H, Dabour Z, Abu-Nassar J, Gal-On A, Aly R (2014) Cucumber mosaic virus as a carotenoid inhibitor reducing Phelipanche aegyptiaca infection in tobacco plants. Plant Signaling & Behavior 9, e972146
| Cucumber mosaic virus as a carotenoid inhibitor reducing Phelipanche aegyptiaca infection in tobacco plants.Crossref | GoogleScholarGoogle Scholar |
Izaguirre-Mayoral ML, Garrido MJ (2010) Propyl gallate, a free radical scavenger, counteracts the benefits of exogenously applied salicylic acid and aggravates the deleterious effects of the Southern bean mosaic virus in Rhizobium-nodulated Phaseolus vulgaris plants. Archives of Phytopathology and Plant Protection 43, 1643–1657.
| Propyl gallate, a free radical scavenger, counteracts the benefits of exogenously applied salicylic acid and aggravates the deleterious effects of the Southern bean mosaic virus in Rhizobium-nodulated Phaseolus vulgaris plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtl2rt7rO&md5=f306b6c7405b0e7f4d58c49b285376a7CAS |
Izaguirre-Mayoral ML, Sinclair TR (2005) Soybean genotypic difference in growth, nutrient accumulation and ultrastructure in response to manganese and iron supply in solution culture. Annals of Botany 96, 149–158.
| Soybean genotypic difference in growth, nutrient accumulation and ultrastructure in response to manganese and iron supply in solution culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXnsVejt7k%3D&md5=d05671f232eb2ca08fcc767d4d1c780dCAS | 15897206PubMed |
Izaguirre-Mayoral ML, Sicardi de Mallorca M, Uzcátegui RC (1989) Comparative response of nodulated and nitrogen supplied cowpea (Vigna unguiculata (L.) Walp var. Tuy) plants to infection by Cowpea mosaic virus. Journal of Experimental Botany 40, 159–165.
| Comparative response of nodulated and nitrogen supplied cowpea (Vigna unguiculata (L.) Walp var. Tuy) plants to infection by Cowpea mosaic virus.Crossref | GoogleScholarGoogle Scholar |
Izaguirre-Mayoral ML, Carballo O, Uzcátegui RC, Sicardi de Mallorca M (1992) Physiological and biochemical aspects of symbiotic nitrogen fixation in cowpea (Vigna unguiculata (L.) Walp. var. Tuy) plants infected by Cowpea mosaic virus. Journal of Experimental Botany 43, 455–462.
| Physiological and biochemical aspects of symbiotic nitrogen fixation in cowpea (Vigna unguiculata (L.) Walp. var. Tuy) plants infected by Cowpea mosaic virus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XktVCgur0%3D&md5=624789ff501255026da11519ed555082CAS |
Izaguirre-Mayoral ML, Carballo O, Sicardi de Mallorca M, Marys E, Gil F (1994) Symbiotic nitrogen fixation and physiological performance of bean (Phaseolus vulgaris L. var. Tacarigua) plants as affected by Rhizobium inoculum position and Bean rugose mosaic virus infection. Journal of Experimental Botany 45, 373–383.
| Symbiotic nitrogen fixation and physiological performance of bean (Phaseolus vulgaris L. var. Tacarigua) plants as affected by Rhizobium inoculum position and Bean rugose mosaic virus infection.Crossref | GoogleScholarGoogle Scholar |
Jáuregui-Zúñiga D, Ortega-Ortega Y, Pedraza-Escalona M, Reyes-Grajeda JP, Ruiz MI, Quinto C (2016) Phosphoproteomic analysis in Phaseolus vulgaris roots treated with Rhizobium etli nodulation factors. Plant Molecular Biology Reporter 34, 961–969.
| Phosphoproteomic analysis in Phaseolus vulgaris roots treated with Rhizobium etli nodulation factors.Crossref | GoogleScholarGoogle Scholar |
Jones RAC (2013) Virus diseases of perennial pasture legumes in Australia: incidences, losses, epidemiology, and management. Crop and Pasture Science 64, 199–215.
| Virus diseases of perennial pasture legumes in Australia: incidences, losses, epidemiology, and management.Crossref | GoogleScholarGoogle Scholar |
Kamaal N, Akram M, Agnihotri AK (2015) Molecular evidence for the association of Tomato leaf curl Gujarat virus with a leaf curl disease of Phaseolus vulgaris L. Journal of Phytopathology 163, 58–62.
| Molecular evidence for the association of Tomato leaf curl Gujarat virus with a leaf curl disease of Phaseolus vulgaris L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitVClsL3L&md5=85b90b49d81594a69f32dedb6a28da03CAS |
Ketelaar T (2013) The actin cytoskeleton in root hairs: all is fine at the tip. Current Opinion in Plant Biology 16, 749–756.
| The actin cytoskeleton in root hairs: all is fine at the tip.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslarur7O&md5=53464cfaa88012fa3c2a65be7241f1e4CAS | 24446547PubMed |
Khalil RR, Bassiouny FM, El-Dougdoug KA, Abo-Elmaty S, Yousef MS (2014) A dramatic physiological and anatomical changes of tomato plants infecting with Tomato yellow leaf curl germinivirus. International Journal of Agricultural Sustainability 10, 1213–1229.
Khan A, Luqman S, Masood N, Singh DK, Saeed ST, Samad A (2016) Eclipta yellow vein virus enhances chlorophyll destruction, singlet oxygen production and alters endogenous redox status in Andrographis paniculata. Plant Physiology and Biochemistry 104, 165–173.
| Eclipta yellow vein virus enhances chlorophyll destruction, singlet oxygen production and alters endogenous redox status in Andrographis paniculata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XltFKjsrk%3D&md5=112870cb3ff056b13c1219a1e24eeff9CAS | 27035255PubMed |
Kothandaraman SV, Devadason A, Ganesan MV (2015) Seed-borne nature of a begomovirus, Mung bean yellow mosaic virus in black gram. Applied Microbiology and Biotechnology 100, 1925–1933.
| Seed-borne nature of a begomovirus, Mung bean yellow mosaic virus in black gram.Crossref | GoogleScholarGoogle Scholar | 26646557PubMed |
Kruk J, Szymańska R, Nowicka B, Dłużewska J (2016) Function of isoprenoid quinones and chromanols during oxidative stress in plants. New Biotechnology 33, 636–643.
| Function of isoprenoid quinones and chromanols during oxidative stress in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XktFKht78%3D&md5=a1d8151ca8bd095fb8867f3f361e37feCAS | 26970272PubMed |
Li H, Ma D, Jin Y, Tu Y, Liu L, Leng C, Dong J, Wang T (2015) Helper component‐proteinase enhances the activity of 1‐deoxy‐d‐xylulose‐5‐phosphate synthase and promotes the biosynthesis of plastidic isoprenoids in Potato virus Y‐infected tobacco. Plant, Cell & Environment 38, 2023–2034.
| Helper component‐proteinase enhances the activity of 1‐deoxy‐d‐xylulose‐5‐phosphate synthase and promotes the biosynthesis of plastidic isoprenoids in Potato virus Y‐infected tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsFGrt7%2FN&md5=f9a6cdf6003727b1c0a4aab3dc7bcdaaCAS |
Liang D, Qu Z, Ma X, Hull R (2005) Detection and localization of Rice stripe virus gene products in vivo. Virus Genes 31, 211–221.
| Detection and localization of Rice stripe virus gene products in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtFyjtbk%3D&md5=45779744c5a5f481bd7e5b911b42a80fCAS | 16025247PubMed |
Liu Y, He C (2016) Regulation of plant reactive oxygen species (ROS) in stress responses: learning from AtRBOHD. Plant Cell Reports 35, 995–1007.
| Regulation of plant reactive oxygen species (ROS) in stress responses: learning from AtRBOHD.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xis1CmsL8%3D&md5=0b1e2e4779fb245187b74431bb438121CAS | 26883222PubMed |
Mabrouk Y, Belhadj O (2016) Enhancing the biological nitrogen fixation of leguminous crops grown under stressed environments. African Journal of Biotechnology 11, 10809–10815.
Muñoz N, Robert G, Melchiorre M, Racca R, Lascano R (2012) Saline and osmotic stress differentially affects apoplastic and intracellular reactive oxygen species production, curling and death of root hair during Glycine max L.–Bradyrhizobium japonicum interaction. Environmental and Experimental Botany 78, 76–83.
| Saline and osmotic stress differentially affects apoplastic and intracellular reactive oxygen species production, curling and death of root hair during Glycine max L.–Bradyrhizobium japonicum interaction.Crossref | GoogleScholarGoogle Scholar |
Muñoz N, Rodriguez M, Robert G, Lascano R (2014a) Negative short-term salt effects on the soybean–Bradyrhizobium japonicum interaction and partial reversion by calcium addition. Functional Plant Biology 41, 96–105.
| Negative short-term salt effects on the soybean–Bradyrhizobium japonicum interaction and partial reversion by calcium addition.Crossref | GoogleScholarGoogle Scholar |
Muñoz N, Soria-Díaz ME, Manyani H, Sánchez-Matamoros RC, Serrano AG, Megías M, Lascano R (2014b) Structure and biological activities of lipochitooligosaccharide nodulation signals produced by Bradyrhizobium japonicum USDA 138 under saline and osmotic stress. Biology and Fertility of Soils 50, 207–215.
| Structure and biological activities of lipochitooligosaccharide nodulation signals produced by Bradyrhizobium japonicum USDA 138 under saline and osmotic stress.Crossref | GoogleScholarGoogle Scholar |
Nagy PD (2016) Tombusvirus–host interactions: co-opted evolutionarily conserved host factors take center court. Annual Review of Virology 3,
| Tombusvirus–host interactions: co-opted evolutionarily conserved host factors take center court.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsFSqtbrO&md5=91cf16d8fe364699be2ba9ed3e0cbdc0CAS | 27578441PubMed |
Ojiewo C, Keatinge DJ, Hughes J, Tenkouano A, Nair R, Varshney R, Siambi M, Monyo E, Ganga-Rao NVPR, Silim S (2015) The role of vegetables and legumes in assuring food, nutrition, and income security for vulnerable groups in sub‐Saharan Africa. World Medical & Health Policy 7, 187–210.
| The role of vegetables and legumes in assuring food, nutrition, and income security for vulnerable groups in sub‐Saharan Africa.Crossref | GoogleScholarGoogle Scholar |
Ovečka M, Berson T, Beck M, Derksen J, Šamaj J, Baluška F, Lichtscheidl IK (2010) Structural sterols are involved in both the initiation and tip growth of root hairs in Arabidopsis thaliana. The Plant Cell 22, 2999–3019.
| Structural sterols are involved in both the initiation and tip growth of root hairs in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 20841426PubMed |
Padmanabhan MS, Kramer SR, Wang X, Culver JN (2008) Tobacco mosaic virus replicase–auxin/indole acetic acid protein interactions: reprogramming the auxin response pathway to enhance virus infection. Journal of Virology 82, 2477–2485.
| Tobacco mosaic virus replicase–auxin/indole acetic acid protein interactions: reprogramming the auxin response pathway to enhance virus infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitlyhurc%3D&md5=81bf01c806ff27c62cf4b6c9d74c4490CAS | 18094187PubMed |
Patiño Y, Garrido MJ (1998) Obtención del antisuero contra el virus del mosaico sureño de la caraota mediante metodología sencilla. Revista de la Facultad de Agronomia de la Universidad del Zulia 15, 319–329.
Pattanayak GK, Tripathy BC (2016) Modulation of biosynthesis of photosynthetic pigments and light-harvesting complex in wild-type and gun5 mutant of Arabidopsis thaliana during impaired chloroplast development. Protoplasma 253, 747–752.
| Modulation of biosynthesis of photosynthetic pigments and light-harvesting complex in wild-type and gun5 mutant of Arabidopsis thaliana during impaired chloroplast development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XkvVGgu74%3D&md5=41e45f9f0b7f87329841a3b144faff97CAS | 27001427PubMed |
Peleg-Grossman S, Volpin H, Levine A (2007) Root hair curling and Rhizobium infection in Medicago truncatula are mediated by phosphatidylinositide-regulated endocytosis and reactive oxygen species. Journal of Experimental Botany 58, 1637–1649.
| Root hair curling and Rhizobium infection in Medicago truncatula are mediated by phosphatidylinositide-regulated endocytosis and reactive oxygen species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsFeisr4%3D&md5=7696c0c1f64f62312fac558cf7909393CAS | 17420174PubMed |
Rathi D, Gayen D, Gayali S, Chakraborty S, Chakraborty N (2016) Legume proteomics: progress, prospects, and challenges. Proteomics 16, 310–327.
| Legume proteomics: progress, prospects, and challenges.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitVCqs7vP&md5=983b7d072bfce7069a482181131ad3b4CAS | 26563903PubMed |
Salem NM, Ehlers JD, Roberts PA, Ng JCK (2010) Biological and molecular diagnosis of seedborne viruses in cowpea germplasm of geographically diverse sub-Saharan origins. Plant Pathology 59, 773–784.
| Biological and molecular diagnosis of seedborne viruses in cowpea germplasm of geographically diverse sub-Saharan origins.Crossref | GoogleScholarGoogle Scholar |
Shabala S, White RG, Djordjevic MA, Ruan YL, Mathesius U (2016) Root-to-shoot signalling: integration of diverse molecules, pathways and functions. Functional Plant Biology 43, 87–104.
| Root-to-shoot signalling: integration of diverse molecules, pathways and functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xos1Wiuw%3D%3D&md5=8260304d8ecc3ec7a3faceeebe3e723bCAS |
Sharman M, Kehoe M, Coutts B, van Leur J, Filardo F, Thomas J (2016) Two complete genome sequences of Phasey bean mild yellows virus, a novel member of the Luteoviridae from Australia. Genome Announcements 4, e01569-15
| Two complete genome sequences of Phasey bean mild yellows virus, a novel member of the Luteoviridae from Australia.Crossref | GoogleScholarGoogle Scholar | 26847905PubMed |
Taiwo LB, Taiwo MA, Shoyinka SA, Jegede SE, Okogun JA, Oyatokun OS, Adebayo GG (2014) Interactive effects of virus and Rhizobium inocula on nodulation, growth and yield of cowpea. International Journal of Plant Physiology and Biochemistry 6, 34–39.
| Interactive effects of virus and Rhizobium inocula on nodulation, growth and yield of cowpea.Crossref | GoogleScholarGoogle Scholar |
Trzmiel K, Zarzyńska-Nowak A, Lewandowska M, Szydło W (2015) Identification of new Brome mosaic virus (BMV) isolates systemically infecting Vigna unguiculata L. European Journal of Plant Pathology 145, 233–238.
Tsukagoshi H (2016) Control of root growth and development by reactive oxygen species. Current Opinion in Plant Biology 29, 57–63.
| Control of root growth and development by reactive oxygen species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvVGnurrN&md5=63c3d202c13b37aa54f097380a031f98CAS | 26724502PubMed |
Uyemoto JK, Grogan RG (1977) Southern bean mosaic virus: evidence for seed transmission in bean embryos. Phytopathology 67, 1190–1196.
| Southern bean mosaic virus: evidence for seed transmission in bean embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXlvFOmsLw%3D&md5=d5a13fcb00fd6d94578b50b5f9f58e01CAS |
Velasquez SM, Barbez E, Kleine-Vehn J, Estevez J (2016) Auxin and cellular elongation. Plant Physiology 170, 1206–1215.
Venturi V, Keel C (2016) Signaling in the rhizosphere. Trends in Plant Science 21, 187–198.
| Signaling in the rhizosphere.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhtF2nsbo%3D&md5=742f84742289b5a8de353c2c83ddc33aCAS | 26832945PubMed |
Verhoeven JThJ, Roenhorst JW, Lesemann D-E, Segundo E, Velasco L, Ruiz L, Janssen D, Cuadrado IM (2003) Southern bean mosaic virus the causal agent of a new disease of Phaseolus vulgaris beans in Spain. European Journal of Plant Pathology 109, 935–941.
| Southern bean mosaic virus the causal agent of a new disease of Phaseolus vulgaris beans in Spain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptVCgtrs%3D&md5=32e7177013b6050fcac525311d53b02fCAS |
Viswanathan C, Anburaj J, Prabu G (2014) Identification and validation of Sugarcane streak mosaic virus-encoded microRNAs and their targets in sugarcane. Plant Cell Reports 33, 265–276.
| Identification and validation of Sugarcane streak mosaic virus-encoded microRNAs and their targets in sugarcane.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1KrtrzF&md5=63c357ff6047fbe58890d6c23df9b935CAS | 24145912PubMed |
Vitti A, Nuzzaci M, Scopa A, Tataranni G, Remans T, Vangronsveld J, Sofo A (2013) Auxin and cytokinin metabolism and root morphological modifications in Arabidopsis thaliana seedlings infected with Cucumber mosaic virus (CMV) or exposed to cadmium. International Journal of Molecular Sciences 14, 6889–6902.
| Auxin and cytokinin metabolism and root morphological modifications in Arabidopsis thaliana seedlings infected with Cucumber mosaic virus (CMV) or exposed to cadmium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlslCnu74%3D&md5=d01037e496f7ae6279f8e2229a6acf1fCAS | 23531542PubMed |
Wang H, Lan P, Shen RF (2016) Integration of transcriptomic and proteomic analysis towards understanding the systems biology of root hairs. Proteomics 16, 877–893.
| Integration of transcriptomic and proteomic analysis towards understanding the systems biology of root hairs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xjs1Gnsbc%3D&md5=3a5a206cf2c3b1d3a46b13e500e1015bCAS | 26749523PubMed |
Wellburn R (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology 144, 307–313.
| The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmsFShsbY%3D&md5=c044468b7d47a2b59a37b74acbdbfbcbCAS |
Wymer CL, Beven AF, Boudonck K, Lloyd CW (1999) Confocal microscopy of plant cells. Methods in Molecular Biology 122, 103–130.
