Pearl millet growth and biochemical alterations determined by mycorrhizal inoculation, water availability and atmospheric CO2 concentration
Eliseu G. Fabbrin A , Yolanda Gogorcena B , Átila F. Mogor A , Idoia Garmendia C and Nieves Goicoechea D E
+ Author Affiliations
- Author Affiliations
A Departamento de Fitotecnia e Fitossanitarismo, Setor de Ciências Agrárias, Universidade Federal do Paraná. Rua dos Funcionários, 1540. Juvevê, Curitiba, PR, Brasil.
B Departamento de Pomología. Estación Experimental de Aula Dei, Consejo Superior de Investigaciones Científicas (CSIC), PO Box 13034, 50080 Zaragoza, Spain.
C Departamento Ciencias de la Tierra y del Medio Ambiente, Facultad de Ciencias, University of Alicante, Carretera San Vicente del Raspeig, s/n Apdo. Correos 99, E-03080 Alicante, Spain.
D Departamento de Biología Ambiental. Grupo de Fisiología del Estrés en Plantas (Unidad Asociada al CSIC, EEAD, Zaragoza e ICVV, Logroño), Facultades de Ciencias y Farmacia, Universidad de Navarra, Irunlarrea 1, 31008, Pamplona, Spain.
E Corresponding author. Email: niegoi@unav.es
Crop and Pasture Science 66(8) 831-840 https://doi.org/10.1071/CP14089
Submitted: 21 March 2014 Accepted: 10 February 2015 Published: 24 July 2015
Abstract
Pearl millet (Pennisetum glaucum L.) is an important fodder and is a potential feedstock for fuel ethanol production in dry areas. Our objectives were to assess the effect of elevated CO2 and/or reduced irrigation on biomass production and levels of sugars and proteins in leaves of pearl millet and to test whether mycorrhizal inoculation could modulate the effects of these abiotic factors on growth and metabolism. Results showed that mycorrhizal inoculation and water regime most influenced biomass of shoots and roots; however, their individual effects were dependent on the atmospheric CO2 concentration. At ambient CO2, mycorrhizal inoculation helped to alleviate effects of water deficit on pearl millet without significant decreases in biomass production, which contrasted with the low biomass of mycorrhizal plants under restricted irrigation and elevated CO2. Mycorrhizal inoculation enhanced water content in shoots, whereas reduced irrigation decreased water content in roots. The triple interaction between CO2, arbuscular mycorrhizal fungi (AMF) and water regime significantly affected the total amount of soluble sugars and determined the predominant soluble sugars in leaves. Under optimal irrigation, elevated CO2 increased the proportion of hexoses in pearl millet that was not inoculated with AMF, thus improving the quality of this plant material for bioethanol production. By contrast, elevated CO2 decreased the levels of proteins in leaves, thus limiting the quality of pearl millet as fodder and primary source for cattle feed.
Additional keywords: arbuscular mycorrhizal fungi, biomass, climatic change, carbohydrates, Pennisetum glaucum, proteins.
References
Andrews DJ, Hanna WW, Rajewski JF, Collins VP (1996) Advances in grain pearl millet: Utilization and production research. In ‘Progress in new crops’. (Ed. J Janick) pp. 170–177. (American Society for Horticultural Science (ASHS) Press: Alexandria, VA, USA)Aranjuelo I, Pérez P, Hernández L, Irigoyen JJ, Zita G, Martínez-Carrasco R, Sánchez-Díaz M (2005) The response of nodulated alfalfa to water supply, temperature and elevated CO2: photosynthetic downregulation. Physiologia Plantarum 123, 348–358.
| The response of nodulated alfalfa to water supply, temperature and elevated CO2: photosynthetic downregulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXis1yhtLk%3D&md5=a4d94d1611c7861d21d23a1cad6e53f6CAS |
Arnon DI, Hoagland DR (1939) A comparison of water culture and soil as media for crop production. Science 89, 512–514.
| A comparison of water culture and soil as media for crop production.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cvnt1Gjug%3D%3D&md5=34d324e407e95783089e8623de77c5f3CAS | 17776587PubMed |
Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11, 3–42.
| Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis.Crossref | GoogleScholarGoogle Scholar |
Barea JM, Pozo MJ, Azcón R, Azcón-Aguilar C (2005) Microbial co-operation in the rhizosphere. Journal of Experimental Botany 56, 1761–1778.
| Microbial co-operation in the rhizosphere.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpvFKnt7g%3D&md5=0afdc141864dc5b4269fcd1cc3d75f84CAS | 15911555PubMed |
Baslam M, Goicoechea N (2012) Water deficit improved the capacity of arbuscular mycorrhizal fungi (AMF) for inducing the accumulation of antioxidant compounds in lettuce leaves. Mycorrhiza 22, 347–359.
| Water deficit improved the capacity of arbuscular mycorrhizal fungi (AMF) for inducing the accumulation of antioxidant compounds in lettuce leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XosFCrt70%3D&md5=7fb6199bfb75bd680294704860318443CAS | 21894519PubMed |
Baslam M, Garmendia I, Goicoechea N (2012) Elevated CO2 may impair the beneficial effect of arbuscular mycorrhizal fungi (AMF) on the mineral and phytochemical quality of lettuce. Annals of Applied Biology 161, 180–191.
| Elevated CO2 may impair the beneficial effect of arbuscular mycorrhizal fungi (AMF) on the mineral and phytochemical quality of lettuce.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVOhu7bE&md5=deb27f6e9329ad5964444da14c9a6b74CAS |
Baslam M, Antolín MC, Gogorcena Y, Muñoz F, Goicoechea N (2014) Changes in alfalfa forage quality and stem carbohydrates induced by arbuscular mycorrhizal fungi and elevated atmospheric CO2. Annals of Applied Biology 164, 190–199.
| Changes in alfalfa forage quality and stem carbohydrates induced by arbuscular mycorrhizal fungi and elevated atmospheric CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXivFOntr8%3D&md5=e191f28408bcd0bcf1a6849ea6b92fa8CAS |
Borde M, Dudhane M, Jite P (2011) Growth, photosynthetic activity and antioxidant responses of mycorrhizal and non-mycorrhizal bajra (Pennisetum glaucum) crop under salinity stress condition. Crop Protection 30, 265–271.
| Growth, photosynthetic activity and antioxidant responses of mycorrhizal and non-mycorrhizal bajra (Pennisetum glaucum) crop under salinity stress condition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhvV2qsL8%3D&md5=fb883394035c1567251662a74f1fd503CAS |
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
| A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=892ed459f97ed9c0a1a4311cd3be3fceCAS | 942051PubMed |
Cavagnaro TR, Gleadow RM, Miller RE (2011) Plant nutrient acquisition and utilization in a high carbon dioxide world. Functional Plant Biology 38, 87–96.
| Plant nutrient acquisition and utilization in a high carbon dioxide world.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVShtLg%3D&md5=ffa9c11465a8c5dbaecf78750610a05cCAS |
de Carvalho AO, Soares DJ, do Carmo MGF, da Costa ACT, Pimentel C (2006) Description of the life-cycle of the pearl millet rust fungus–Puccinia substriata var. penicillariae with a proposal of reducing var. indica to a synonym. Mycopathologia 161, 331–336.
| Description of the life-cycle of the pearl millet rust fungus–Puccinia substriata var. penicillariae with a proposal of reducing var. indica to a synonym.Crossref | GoogleScholarGoogle Scholar |
De Luis I, Irigoyen JJ, Sánchez-Díaz M (1999) Elevated CO2 enhances plant growth in droughted N2-fixing alfalfa without improving water status. Physiologia Plantarum 107, 84–89.
| Elevated CO2 enhances plant growth in droughted N2-fixing alfalfa without improving water status.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXnsVGmsbc%3D&md5=6ae8032414730108ee7d6cec662e3225CAS |
Dien BS, Jung HG, Vogel KP, Casler MD, Lamb JFS, Weimer PJ, Iten L, Mitchell RB, Sarath G (2006) Chemical composition and response to dilute-acid pretreatment and enzymatic saccharification of alfalfa, reed canarygrass, and switchgrass. Biomass and Bioenergy 30, 880–891.
| Chemical composition and response to dilute-acid pretreatment and enzymatic saccharification of alfalfa, reed canarygrass, and switchgrass.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVSis7jO&md5=ff393efdac05b9a52421c3b9740c2997CAS |
Dien BS, Miller DJ, Hector RE, Dixon RA, Chen F, McCaslin M, Reisen P, Sarath G, Cotta MA (2011) Enhancing alfalfa conversion efficiencies for sugar recovery and ethanol production by altering lignin composition. Bioresource Technology 102, 6479–6486.
| Enhancing alfalfa conversion efficiencies for sugar recovery and ethanol production by altering lignin composition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlsVygt7o%3D&md5=6278bca82a1bd7f45886f8a26fc6d145CAS | 21474304PubMed |
Drake BG, González-Meler MA, Long SP (1997) More efficient plants: a consequence of rising atmospheric CO2. Annual Review of Plant Physiology and Plant Molecular Biology 48, 609–639.
| More efficient plants: a consequence of rising atmospheric CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjs1eltbY%3D&md5=75f1fa57e6b50882c98ade2bddfb3044CAS | 15012276PubMed |
FAOSTAT 2015 http://faostat3.fao.org
Ghannoum O, von Caemmerer S, Ziska LH, Conroy JP (2000) The growth response of C4 plants to rising atmospheric CO2 partial pressure: a reassessment. Plant, Cell & Environment 23, 931–942.
| The growth response of C4 plants to rising atmospheric CO2 partial pressure: a reassessment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXntFGjsb8%3D&md5=7f3a6eb0e92b0a8bc70c5fabb4bcbd96CAS |
Goicoechea N, Antolín MC, Sánchez-Díaz M (1997) Influence of arbuscular mycorrhizae and Rhizobium on nutrient content and water relations in drought stressed alfalfa. Plant and Soil 192, 261–268.
| Influence of arbuscular mycorrhizae and Rhizobium on nutrient content and water relations in drought stressed alfalfa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmtFGrsrg%3D&md5=02bb7b5b52039975d88ecd5756fc2aa5CAS |
Goicoechea N, Merino S, Sánchez-Díaz M (2004) Contribution of arbuscular mycorrhizal fungi (AMF) to the adaptations exhibited by the deciduous shrub Anthyllis cytisoides under water deficit. Physiologia Plantarum 122, 453–464.
| Contribution of arbuscular mycorrhizal fungi (AMF) to the adaptations exhibited by the deciduous shrub Anthyllis cytisoides under water deficit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFelug%3D%3D&md5=4b7e17733d58b48e98006d74019ef4e4CAS |
Gregory JM, Mitchell JFB, Brady AJ (1997) Summer drought in northern midlatitudes in a time-dependent CO2 climate experiment. Journal of Climate 10, 662–686.
| Summer drought in northern midlatitudes in a time-dependent CO2 climate experiment.Crossref | GoogleScholarGoogle Scholar |
Hamerlynck EP, McAllister CA, Knapp AK, Ham JM, Owensby CE (1997) Photosynthetic gas exchange and water relation responses of three tallgrass prairie species to elevated carbon dioxide and moderate drought. International Journal of Plant Sciences 158, 608–616.
| Photosynthetic gas exchange and water relation responses of three tallgrass prairie species to elevated carbon dioxide and moderate drought.Crossref | GoogleScholarGoogle Scholar |
Irigoyen JJ, Emerich DW, Sánchez-Díaz M (1992) Water stress induced changes in concentrations or proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants. Physiologia Plantarum 84, 55–60.
| Water stress induced changes in concentrations or proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XhslSgs74%3D&md5=a4c1aad4c05bfa3ff8bd959c8a7905a7CAS |
Jarvis CE, Walker JRL (1993) Simultaneous, rapid, spectrophotometric determination of total starch, amylose and amylopectin. Journal of the Science of Food and Agriculture 63, 53–57.
| Simultaneous, rapid, spectrophotometric determination of total starch, amylose and amylopectin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXivFKhsQ%3D%3D&md5=e8e061009bb230157e1f289748cc9795CAS |
Jiménez S, Ollat N, Deborde C, Maucourt M, Rellán-Álvarez R, Moreno MA, Gogorcena Y (2011) Metabolic response in roots of Prunus rootstocks submitted to iron chlorosis. Journal of Plant Physiology 168, 415–423.
| Metabolic response in roots of Prunus rootstocks submitted to iron chlorosis.Crossref | GoogleScholarGoogle Scholar | 20952094PubMed |
Kohler J, Caravaca F, Alguacil MM, Roldán A (2009) Elevated CO2 increases the effect of an arbuscular mycorrhizal fungus and a plant-growth-promoting rhizobacterium on structural stability of a semiarid agricultural soil under drought conditions. Soil Biology & Biochemistry 41, 1710–1716.
| Elevated CO2 increases the effect of an arbuscular mycorrhizal fungus and a plant-growth-promoting rhizobacterium on structural stability of a semiarid agricultural soil under drought conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXoslGjsbo%3D&md5=1e739a32aaa8b19eadaa632fa87d8fb2CAS |
Krishna KR, Shetty KG, Dart PJ, Andrews DJ (1985) Genotype dependent variation in mycorrhizal colonization and response to inoculation of pearl millet. Plant and Soil 86, 113–125.
| Genotype dependent variation in mycorrhizal colonization and response to inoculation of pearl millet.Crossref | GoogleScholarGoogle Scholar |
Krüger M, Krüger C, Walker C, Stockinger H, Schüßle A (2012) Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytologist 193, 970–984.
| Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level.Crossref | GoogleScholarGoogle Scholar | 22150759PubMed |
Lara MV, Andreo CS (2011) C4 plants adaptation to high levels of CO2 and to drought environments. In ‘Abiotic stress in plants—Mechanisms and adaptations’. (Ed. A Shanker) (InTech: Rijeka, Croatia) Available at: www.intechopen.com/books/abiotic-stress-in-plants-mechanisms-and-adaptations/c4-plants-adaptation-to-high-levels-of-co2-and-to-drought-environments
Maiti R, Wesche-Ebeling P (1997) ‘Pearl millet science.’ (Science Publishers, Inc.: Enfield, NH, USA)
Markelz RJC, Strellner RS, Leakey ADB (2011) Impairment of C4 photosynthesis by drought is exacerbated by limiting nitrogen and ameliorated by elevated [CO2] in maize. Journal of Experimental Botany 62, 3235–3246.
| Impairment of C4 photosynthesis by drought is exacerbated by limiting nitrogen and ameliorated by elevated [CO2] in maize.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsFWjt7w%3D&md5=b64558b122eb9a1019de7996f77854bfCAS |
Mohammad MJ, Pan WL, Kennedy AC (1998) Seasonal mycorrhizal colonization of winter wheat and its effect on wheat growth under dryland field conditions. Mycorrhiza 8, 139–144.
| Seasonal mycorrhizal colonization of winter wheat and its effect on wheat growth under dryland field conditions.Crossref | GoogleScholarGoogle Scholar |
Mohan JE, Cowden CC, Baas P, Dawadi A, Frankson PT, Helmick K, Hughes E, Khan S, Lang A, Machmuller M, Taylor M, Witt A (2014) Mycorrhizal fungi mediation of terrestrial ecosystem responses to global change: mini-review. Fungal Ecology 10, 3–19.
| Mycorrhizal fungi mediation of terrestrial ecosystem responses to global change: mini-review.Crossref | GoogleScholarGoogle Scholar |
Netto DAM (1998) A cultura do milheto. Comunicado Técnico 11. EMBRAPA-Centro Nacional de Pesquisa de Milho e Sorgo, Sete Lagoas, MG, Brasil.
Oliveira VF, Zaindan LBP, Braga MR, Aidar MPM, Carvalho MAM (2010) Elevated CO2 atmosphere promotes plants growth and inulin production in the cerrado species Vernonia herbacea. Functional Plant Biology 37, 223–231.
| Elevated CO2 atmosphere promotes plants growth and inulin production in the cerrado species Vernonia herbacea.Crossref | GoogleScholarGoogle Scholar |
Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society 55, 158–161.
| Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection.Crossref | GoogleScholarGoogle Scholar |
Purseglove JW (1972) ‘Tropical crops: monocotyledons.’ (Longman: New York)
Rawson HM, Gifford RM, Condon BN (1995) Temperature gradient chambers for research on global environment change. I. Portable chambers for research on short-stature vegetation. Plant, Cell & Environment 18, 1048–1054.
| Temperature gradient chambers for research on global environment change. I. Portable chambers for research on short-stature vegetation.Crossref | GoogleScholarGoogle Scholar |
Sánchez-Díaz M, Pardo M, Antolín MC, Peña J, Aguirreolea J (1990) Effect of water stress on photosynthetic activity in the Medicago–Rhizobium–Glomus symbiosis. Plant Science 71, 215–221.
| Effect of water stress on photosynthetic activity in the Medicago–Rhizobium–Glomus symbiosis.Crossref | GoogleScholarGoogle Scholar |
Sanz-Sáez A, Erice G, Aguirreolea J, Muñoz F, Sánchez-Díaz M, Irigoyen JJ (2012) Alfalfa forage digestibility, quality and yield under future climate change scenarios vary with Sinorhizobium meliloti strain. Journal of Plant Physiology 169, 782–788.
| Alfalfa forage digestibility, quality and yield under future climate change scenarios vary with Sinorhizobium meliloti strain.Crossref | GoogleScholarGoogle Scholar | 22369772PubMed |
Schüβler A, Schwarzott D, Walker C (2001) A new phylum, the Glomeromycota: phylogeny and evolution. Mycological Research 105, 1413–1421.
| A new phylum, the Glomeromycota: phylogeny and evolution.Crossref | GoogleScholarGoogle Scholar |
Seki M, Umezawa T, Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Current Opinion in Plant Biology 10, 296–302.
Smith SE, Read DJ (2008) ‘Mycorrhizal symbiosis.’ 3rd edn (Academic Press: London)
Winkel T, Renno JF, Payne WA (1997) Effect of the timing of water deficit on growth, phenology and yield of pearl millet (Pennisetum glaucum (L.) R. Br.) grown in Sahelian conditions. Journal of Experimental Botany 48, 1001–1009.
| Effect of the timing of water deficit on growth, phenology and yield of pearl millet (Pennisetum glaucum (L.) R. Br.) grown in Sahelian conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXks1artbc%3D&md5=d228c94a3fe4d1a10c0ebfeb82127206CAS |
Winkel T, Payne W, Renno JF (2001) Ontogeny modifies the effect of water stress on stomatal control, leaf area duration and biomass partitioning of Pennisetum glaucum. New Phytologist 149, 71–82.
| Ontogeny modifies the effect of water stress on stomatal control, leaf area duration and biomass partitioning of Pennisetum glaucum.Crossref | GoogleScholarGoogle Scholar |
Wu X, Wang D, Bean SR, Wilson JP (2006) Ethanol production from pearl millet using Saccharomyces cerevisiae. Cereal Chemistry 83, 127–131.
| Ethanol production from pearl millet using Saccharomyces cerevisiae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjs1Smtrs%3D&md5=465b202b0553a57117b94b470abef23bCAS |
Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Research 14, 415–421.
| A decimal code for the growth stages of cereals.Crossref | GoogleScholarGoogle Scholar |
