Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Anatomical, morphological and growth responses of Thinopyrum ponticum plants subjected to partial and complete submergence during early stages of development

María del Rosario M. Iturralde Elortegui https://orcid.org/0000-0003-2456-812X A F , Germán D. Berone B C , Gustavo G. Striker D E , María J. Martinefsky A , María G. Monterubbianesi C and Silvia G. Assuero C
+ Author Affiliations
- Author Affiliations

A Instituto Nacional de Tecnología Agropecuaria (INTA), AER Olavarría, Alsina 2642, B7400COJ Olavarría, Buenos Aires, Argentina.

B Instituto Nacional de Tecnología Agropecuaria (INTA), EEA Balcarce, Ruta Nacional 226 km 73.5, C.C. 276, B7620BKL Balcarce, Buenos Aires, Argentina.

C Facultad de Ciencias Agrarias, Universidad Nacional de Mar del Plata, Ruta Nacional 226 km 73.5, C.C. 276, B7620BKL Balcarce, Buenos Aires, Argentina.

D IFEVA, Universidad de Buenos Aires, CONICET, Facultad de Agronomía, Buenos Aires, Argentina, Av. San Martín 4453, CPA 1417, DSE Buenos Aires, Argentina.

E UWA School of Agriculture and Environment, Faculty of Science, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.

F Corresponding author. Email: iturraldeelortegui.m@inta.gob.ar

Functional Plant Biology 47(8) 757-768 https://doi.org/10.1071/FP19170
Submitted: 11 June 2019  Accepted: 25 March 2020   Published: 29 May 2020

Abstract

Seedling recruitment and growth of forage grasses in flood-prone grasslands is often impaired by submergence. We evaluate the responses of Thinopyrum ponticum (Podp.) Barkw. & Dewey to partial and complete submergence at two early stages of development. Two greenhouse experiments were carried out with plants at three expanded leaves (Experiment 1) or five expanded leaves stage (Experiment 2). In each case, three treatments were applied for 14 days: control (C), partial submergence (PS; water level to half plant height), and complete submergence (CS; water level to 1.5 times plant height). Submergence was followed by a recovery period of 14 days at well drained conditions. Assessments included plant survival, height, leaf blade and pseudostem length, soluble carbohydrates in pseudostem, and shoot and root dry mass accumulation at the beginning and end of the submergence, and at the end of the recovery period. Root aerenchyma formation was determined on day 14 in both experiments. Under PS all plants survived, and the impact of the stress was related to the plants’ developmental stage. However, plants with five expanded leaves increased total plant biomass with respect to control by 48%, plants with three expanded leaves reduced it by the same percentage. This response could be related to a higher ability to form root aerenchyma (17 vs 10%), and an enhanced leaf de-submergence capacity due to promoted leaf blade and pseudostem lengthening. Complete submergence treatment compromised the survival of 70% of the individuals with three expanded leaves but did not affect the survival at the five expanded leaves stage. In any developmental stage (three or five expanded leaves) plants fail to promote enough elongation of leaf blades or pseudostems to emerge from the water, so that always remained below the water surface. Root aerenchyma was not increased by CS at either of these two plant developmental stages. The high amount and concentration of pseudostem total soluble carbohydrates of the larger (five expanded leaves) plants facilitated their recovery growth after submergence. Our results predict the successful introduction of this species in areas where water excesses can cause soil waterlogging or shallow-partial plant submergence, but suggest avoidance of areas prone to suffer high-intensity flooding that lead to full plant submergence as this would highly constrain plant recruitment.

Additional keywords: plant developmental stage, plant survival, recovery, root aerenchyma formation, soluble carbohydrates.


References

Anderson ER (1972) Flooding tolerance of Panicum coloratum. Queensland Journal of Agricultural and Animal Sciences 29, 173–179.

Armstrong W (1979) Aeration in higher plants. Advances in Botanical Research 7, 225–332.
Aeration in higher plants.Crossref | GoogleScholarGoogle Scholar |

Ashraf M (2003) Relationships between leaf gas exchange characteristics and growth of differently adapted populations of blue panicgrass (Panicum antidotale Retz.) under salinity or waterlogging. Plant Science 165, 69–75.
Relationships between leaf gas exchange characteristics and growth of differently adapted populations of blue panicgrass (Panicum antidotale Retz.) under salinity or waterlogging.Crossref | GoogleScholarGoogle Scholar |

Bailey-Serres J, Voesenek LACJ (2008) Flooding stress: acclimations and genetic diversity. Annual Review of Plant Biology 59, 313–339.
Flooding stress: acclimations and genetic diversity.Crossref | GoogleScholarGoogle Scholar | 18444902PubMed |

Bailey–Serres J, Voesenek LACJ (2010) Life in the balance: a signaling network controlling survival of flooding. Current Opinion in Plant Biology 13, 489–494.
Life in the balance: a signaling network controlling survival of flooding.Crossref | GoogleScholarGoogle Scholar | 20813578PubMed |

Barkworth ME, Anderton LK, Capels KM, Long S, Piep MB (2007) ‘Manual of grasses for North America.’ (University Press of Colorado: Boulder, CO, USA)

Baruch Z (1994) Responses to drought and flooding in tropical forage grasses: II. Leaf water potential, photosynthesis rate and alcohol dehydrogenase activity. Plant and Soil 164, 97–105.
Responses to drought and flooding in tropical forage grasses: II. Leaf water potential, photosynthesis rate and alcohol dehydrogenase activity.Crossref | GoogleScholarGoogle Scholar |

Bennett SJ, Barrett-Lennard EG, Colmer TD (2009) Salinity and waterlogging as constraints to saltland pasture production: a review. Agriculture, Ecosystems & Environment 129, 349–360.
Salinity and waterlogging as constraints to saltland pasture production: a review.Crossref | GoogleScholarGoogle Scholar |

Borrajo CI, Sánchez-Moreiras AM, Reigosa MJ (2018) Morpho-physiological responses of tall wheatgrass populations to different levels of water stress. PLoS One 13, e0209281
Morpho-physiological responses of tall wheatgrass populations to different levels of water stress.Crossref | GoogleScholarGoogle Scholar | 30557312PubMed |

Chen X, Huber H, De Kroon H, Peeters AJM, Poorter H, Voesenek LACJ, Visser EJW (2009) Intraspecific variation in the magnitude and pattern of flooding-induced shoot elongation in Rumex palustris. Annals of Botany 104, 1057–1067.
Intraspecific variation in the magnitude and pattern of flooding-induced shoot elongation in Rumex palustris.Crossref | GoogleScholarGoogle Scholar | 19687030PubMed |

Chen X, Visser EJW, De Kroon H, Pierik R, Voesenek LACJ, Huber H (2011) Fitness consequences of natural variation in flooding-induced shoot elongation in Rumex palustris. New Phytologist 190, 409–420.
Fitness consequences of natural variation in flooding-induced shoot elongation in Rumex palustris.Crossref | GoogleScholarGoogle Scholar | 21261627PubMed |

Colmer TD (2003) Aerenchyma and an inducible barrier to radial oxygen loss facilitate root aeration in upland, paddy and deepwater rice (Oryza sativa L.). Annals of Botany 91, 301–309.
Aerenchyma and an inducible barrier to radial oxygen loss facilitate root aeration in upland, paddy and deepwater rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 12509350PubMed |

Colmer TD, Pedersen O (2008) Underwater photosynthesis and respiration in leaves of submerged wetland plants: gas films improve CO2 and O2 exchange. New Phytologist 177, 918–926.
Underwater photosynthesis and respiration in leaves of submerged wetland plants: gas films improve CO2 and O2 exchange.Crossref | GoogleScholarGoogle Scholar | 18086222PubMed |

Colmer TD, Voesenek LACJ (2009) Flooding tolerance: suites of plant traits in variable environments. Functional Plant Biology 36, 665–681.
Flooding tolerance: suites of plant traits in variable environments.Crossref | GoogleScholarGoogle Scholar |

Crawford RMM (2003) Seasonal differences in plant responses to flooding and anoxia. Canadian Journal of Botany 81, 1224–1246.
Seasonal differences in plant responses to flooding and anoxia.Crossref | GoogleScholarGoogle Scholar |

Davies A (1988) The regrowth of grass swards. In ‘The grass crop’. pp. 85–127. (Springer: Dordrecht, Netherlands)

Di Bella CE, Striker GG, Loreti J, Cosentino DJ, Grimoldi AA (2016) Soil water regime of grassland communities along subtle topographic gradient in the flooding pampa (Argentina). Soil and Water Research 11, 90–96.
Soil water regime of grassland communities along subtle topographic gradient in the flooding pampa (Argentina).Crossref | GoogleScholarGoogle Scholar |

Dubois M, Gilles KA, Hamilton JK, Rebers P, Smith F (1956) Colorimetric method for determination of sugars and related substances. Analytical Chemistry 28, 350–356.
Colorimetric method for determination of sugars and related substances.Crossref | GoogleScholarGoogle Scholar |

Falasca SL, Miranda C, Alvarez SP (2017) Agro-ecological zoning for tall wheatgrass (Thinopyrum Ponticum) as a potential energy and forage crop in salt-affected and dry lands of Argentina. Scientific Pages of Crop Science 1, 10–19.

Fukao T, Xu K, Ronald PC, Bailey-Serres J (2006) A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. The Plant Cell 18, 2021–2034.
A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice.Crossref | GoogleScholarGoogle Scholar | 16816135PubMed |

Grimoldi AA, Insausti P, Roitman GG, Soriano A (1999) Responses to flooding intensity in Leontodon taraxacoides. New Phytologist 141, 119–128.
Responses to flooding intensity in Leontodon taraxacoides.Crossref | GoogleScholarGoogle Scholar |

Grimoldi AA, Insausti P, Vasellati V, Striker GG (2005) Constitutive and plastic root traits and their role in differential tolerance to soil flooding among coexisting species of lowland grassland. International Journal of Plant Sciences 166, 805–813.
Constitutive and plastic root traits and their role in differential tolerance to soil flooding among coexisting species of lowland grassland.Crossref | GoogleScholarGoogle Scholar |

Hattori Y, Nagai K, Furukawa S, Song XJ, Kawano R, Sakakibara H, Wu J, Matsumoto T, Yoshimura A, Kitano H, Matsuoka M, Mori H, Ashikari M (2009) The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 460, 1026–1030.
The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water.Crossref | GoogleScholarGoogle Scholar | 19693083PubMed |

Hunt R (1982) ‘Plant growth curves. The functional approach to plant growth analysis.’ (E. Arnold Publishers: London, UK)

Imaz JA, Gimenez DO, Grimoldi AA, Striker GG (2012) The effects of submergence on anatomical, morphological and biomass allocation responses of tropical grasses Chloris gayana and Panicum coloratum at seedling stage. Crop and Pasture Science 63, 1145–1155.
The effects of submergence on anatomical, morphological and biomass allocation responses of tropical grasses Chloris gayana and Panicum coloratum at seedling stage.Crossref | GoogleScholarGoogle Scholar |

Imaz JA, Gimenez DO, Grimoldi AA, Striker GG (2015) High recovery ability overrides the negative effects of flooding on growth of tropical grasses Chloris gayana and Panicum coloratum. Crop and Pasture Science 66, 100–106.
High recovery ability overrides the negative effects of flooding on growth of tropical grasses Chloris gayana and Panicum coloratum.Crossref | GoogleScholarGoogle Scholar |

Insausti P, Grimoldi AA, Chaneton EJ, Vasellati V (2001) Flooding induces a suite of adaptive plastic responses in the grass Paspalum dilatatum. New Phytologist 152, 291–299.
Flooding induces a suite of adaptive plastic responses in the grass Paspalum dilatatum.Crossref | GoogleScholarGoogle Scholar |

IPCC (2014) Summary for policymakers. In ‘Climate change 2014: impacts, adaptation, and vulnerability. Part A: Global and sectoral aspects. Contribution of Working Group II to the Fifth 56 Assessment Report of the Intergovernmental Panel on Climate Change’. (Eds CB Field, VR Barros, DJ Dokken, KJ Mach, MD Mastrandrea, TE Bilir, LL White) pp. 1–32. (Cambridge University Press: Cambridge, UK)

Jackson MB, Armstrong W (1999) Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence. Plant Biology 1, 274–287.
Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence.Crossref | GoogleScholarGoogle Scholar |

Jackson MB, Ram PC (2003) Physiological and molecular basis of susceptibility and tolerance of rice plants to complete submergence. Annals of Botany 91, 227–241.
Physiological and molecular basis of susceptibility and tolerance of rice plants to complete submergence.Crossref | GoogleScholarGoogle Scholar | 12509343PubMed |

Jenkins S (2007) Ecophysiological principles governing the zonation of Puccinellia (Puccinellia ciliata) and tall wheatgrass (Thinopyrum ponticum) on saline waterlogged land in south-western Australia. PhD thesis. School of Earth and Geographical Sciences, Faculty of Natural and Agricultural Sciences, University of Western Australia, Perth, WA, Australia.

Jenkins S, Barrett-Lennard EG, Rengel Z (2010) Impacts of waterlogging and salinity on puccinellia (Puccinellia ciliata) and tall wheatgrass (Thinopyrum ponticum): zonation on saltland with a shallow water-table, plant growth, and Na+ and K+ concentrations in the leaves. Plant and Soil 329, 91–104.
Impacts of waterlogging and salinity on puccinellia (Puccinellia ciliata) and tall wheatgrass (Thinopyrum ponticum): zonation on saltland with a shallow water-table, plant growth, and Na+ and K+ concentrations in the leaves.Crossref | GoogleScholarGoogle Scholar |

Justin SHFW, Armstrong W (1987) The anatomical characteristics of roots and plant response to soil flooding. New Phytologist 106, 465–495.
The anatomical characteristics of roots and plant response to soil flooding.Crossref | GoogleScholarGoogle Scholar |

Kreuzwieser J, Gessler A (2010) Global climate change and tree nutrition: influence of water availability. Tree Physiology 30, 1221–1234.
Global climate change and tree nutrition: influence of water availability.Crossref | GoogleScholarGoogle Scholar | 20581013PubMed |

Laan P, Tosserams M, Blom CWPM, Veen BW (1990) Internal oxygen transport in Rumex species and its significance for respiration under hypoxic conditions. Plant and Soil 122, 39–46.
Internal oxygen transport in Rumex species and its significance for respiration under hypoxic conditions.Crossref | GoogleScholarGoogle Scholar |

Maas EV (1986) Salt tolerance of plants. Applied Agricultural Research 1, 12–26.

Manzur ME (2012) Bases ecofisiológicas relacionadas con la tolerancia a la inundación y la defoliación en especies conspicuas de pastizales húmedos. PhD thesis. Universidad Nacional de Buenos Aires, Facultad de Agronomía, Argentina.

Manzur ME, Grimoldi AA, Insausti P, Striker GG (2009) Escape from water or remain quiescent? Lotus tenuis changes its strategy depending on depth of submergence. Annals of Botany 104, 1163–1169.
Escape from water or remain quiescent? Lotus tenuis changes its strategy depending on depth of submergence.Crossref | GoogleScholarGoogle Scholar | 19687031PubMed |

Mommer L, Visser EJW (2005) Underwater photosynthesis in flooded terrestrial plants: a matter of leaf plasticity. Annals of Botany 96, 581–589.
Underwater photosynthesis in flooded terrestrial plants: a matter of leaf plasticity.Crossref | GoogleScholarGoogle Scholar | 16024559PubMed |

Mommer L, Pons TL, Visser EJW (2006) Photosynthetic consequences of phenotypic plasticity in response to submergence: Rumex palustris as a case study. Journal of Experimental Botany 57, 283–290.
Photosynthetic consequences of phenotypic plasticity in response to submergence: Rumex palustris as a case study.Crossref | GoogleScholarGoogle Scholar | 16291797PubMed |

Pedersen O, Perata P, Voesenek LACJ (2017) Flooding and low oxygen responses in plants. Functional Plant Biology 44, iii–vi.
Flooding and low oxygen responses in plants.Crossref | GoogleScholarGoogle Scholar |

Ploschuk RA, Grimoldi AA, Ploschuk EL, Striker GG (2017) Growth during recovery evidences the waterlogging tolerance of forage grasses. Crop and Pasture Science 68, 574–582.
Growth during recovery evidences the waterlogging tolerance of forage grasses.Crossref | GoogleScholarGoogle Scholar |

R Core Team (2014) R: A language and environment for statistical computing. (R Foundation for Statistical Computing, Vienna, Austria) Available at http://www.R-project.org/. [Verified 17 May 2020]

Ram PC, Singh BB, Singh AK, Ram P, Singh PN, Singh HP, Singh RK (2002) Submergence tolerance in rainfed lowland rice: physiological basis and prospects for cultivar improvement through marker–aided breeding. Field Crops Research 76, 131–152.
Submergence tolerance in rainfed lowland rice: physiological basis and prospects for cultivar improvement through marker–aided breeding.Crossref | GoogleScholarGoogle Scholar |

San Celedonio RP, Abeledo LG, Miralles DJ (2014) Identifying the critical period for waterlogging on yield and its components in wheat and barley. Plant and Soil 378, 265–277.
Identifying the critical period for waterlogging on yield and its components in wheat and barley.Crossref | GoogleScholarGoogle Scholar |

San Celedonio RP, Abeledo LG, Mantese AI, Miralles DJ (2017) Differential root and shoot biomass recovery in wheat and barley with transient waterlogging during preflowering. Plant and Soil 417, 481–498.
Differential root and shoot biomass recovery in wheat and barley with transient waterlogging during preflowering.Crossref | GoogleScholarGoogle Scholar |

Sand-Jensen K (1989) Environmental variables and their effect on photosynthesis of aquatic plant communities. Aquatic Botany 34, 5–25.
Environmental variables and their effect on photosynthesis of aquatic plant communities.Crossref | GoogleScholarGoogle Scholar |

Scheinost P, Tilley D, Ogle D, Stannard M (2008) Tall wheatgrass plant guide. NRCS plants database. National Plant Data Centre, Baton Rouge. Available at https://plants.usda.gov/plantguide/pdf/pg_thpo7.pdf [Verified 31 January 2020]

Schindelin J, Arganda-carreras I, Frise E (2012) Fiji: an open-source platform for biological-image analysis Nature Methods 9, 676–682.
Fiji: an open-source platform for biological-image analysisCrossref | GoogleScholarGoogle Scholar | 22743772PubMed |

Seago JL, Marsh LC, Stevens KJ, Soukup A, Votrubová O, Enstone DE (2005) A re-examination of the root cortex in wetland flowering plants with respect to aerenchyma. Annals of Botany 96, 565–579.
A re-examination of the root cortex in wetland flowering plants with respect to aerenchyma.Crossref | GoogleScholarGoogle Scholar | 16081497PubMed |

Setter TL, Laureles EV (1996) The beneficial effect of reduced elongation growth on submergence tolerance of rice. Journal of Experimental Botany 47, 1551–1559.
The beneficial effect of reduced elongation growth on submergence tolerance of rice.Crossref | GoogleScholarGoogle Scholar |

Striker GG (2012) Time is on our side: the importance of considering a recovery period when assessing flooding tolerance in plants. Ecological Research 27, 983–987.
Time is on our side: the importance of considering a recovery period when assessing flooding tolerance in plants.Crossref | GoogleScholarGoogle Scholar |

Striker GG, Colmer TD (2017) Flooding tolerance of forage legumes. Journal of Experimental Botany 68, 1851–1872.
Flooding tolerance of forage legumes.Crossref | GoogleScholarGoogle Scholar | 27325893PubMed |

Striker GG, Insausti P, Grimoldi AA, Ploschuk EL, Vasellati V (2005) Physiological and anatomical basis of differential tolerance to soil flooding of Lotus corniculatus L. and Lotus glaber Mill. Plant and Soil 276, 301–311.
Physiological and anatomical basis of differential tolerance to soil flooding of Lotus corniculatus L. and Lotus glaber Mill.Crossref | GoogleScholarGoogle Scholar |

Striker GG, Insausti P, Grimoldi AA, Vega AS (2007) Trade-off between root porosity and mechanical strength in species with different types of aerenchyma. Plant, Cell & Environment 30, 580–589.
Trade-off between root porosity and mechanical strength in species with different types of aerenchyma.Crossref | GoogleScholarGoogle Scholar |

Striker GG, Manzur ME, Grimoldi AA (2011) Increasing defoliation frequency constrains regrowth of Lotus tenuis under flooding. The role of crown reserves. Plant and Soil 343, 261–272.
Increasing defoliation frequency constrains regrowth of Lotus tenuis under flooding. The role of crown reserves.Crossref | GoogleScholarGoogle Scholar |

Striker GG, Izaguirre RF, Manzur ME, Grimoldi AA (2012) Different strategies of Lotus japonicus, L. corniculatus and L. tenuis to deal with complete submergence at seedling stage. Plant Biology 14, 50–55.

Striker GG, Casas C, Kuang X, Grimoldi AA (2017) No escape? Costs and benefits of leaf de-submergence in the pasture grass Chloris gayana under different flooding regimes. Functional Plant Biology 44, 899–906.
No escape? Costs and benefits of leaf de-submergence in the pasture grass Chloris gayana under different flooding regimes.Crossref | GoogleScholarGoogle Scholar |

Striker GG, Kotula L, Colmer TD (2019) Tolerance to partial and complete submergence in the forage legume: an evaluation of 15 accessions for petiole hyponastic response and gas-filled spaces, leaf hydrophobicity and gas films, and root phellem. Annals of Botany 123, 169–180.
Tolerance to partial and complete submergence in the forage legume: an evaluation of 15 accessions for petiole hyponastic response and gas-filled spaces, leaf hydrophobicity and gas films, and root phellem.Crossref | GoogleScholarGoogle Scholar | 30124766PubMed |

Teakle NL, Bazihizina N, Shabala S, Colmer TD, Barrett-Lennard EG, Rodrigo Moreno A, Läuchli AE (2013) Differential tolerance to combined salinity and O2 deficiency in the halophytic grasses Puccinellia ciliata and Thinopyrum ponticum: the importance of K+ retention in roots. Environmental and Experimental Botany 87, 69–78.
Differential tolerance to combined salinity and O2 deficiency in the halophytic grasses Puccinellia ciliata and Thinopyrum ponticum: the importance of K+ retention in roots.Crossref | GoogleScholarGoogle Scholar |

Thomas H, James AR (1999) Partitioning of sugars in Lolium perenne (perennial ryegrass) during drought and on rewatering. New Phytologist 142, 295–305.
Partitioning of sugars in Lolium perenne (perennial ryegrass) during drought and on rewatering.Crossref | GoogleScholarGoogle Scholar |

Thorne GN (1959) Photosynthesis of lamina and sheath of barley leaves. Annals of Botany 23, 365–370.
Photosynthesis of lamina and sheath of barley leaves.Crossref | GoogleScholarGoogle Scholar |

Vashisht D, Hesselink A, Pierik R, Ammerlaan JMH, Bailey-Serres J, Visser EJW, Sasidharan R (2011) Natural variation of submergence tolerance among Arabidopsis thaliana accessions. New Phytologist 190, 299–310.
Natural variation of submergence tolerance among Arabidopsis thaliana accessions.Crossref | GoogleScholarGoogle Scholar | 21108648PubMed |

Voesenek LACJ, Sasidharan R (2013) Ethylene – and oxygen signalling – drive plant survival during flooding. Plant Biology 15, 426–435.
Ethylene – and oxygen signalling – drive plant survival during flooding.Crossref | GoogleScholarGoogle Scholar |

Voesenek LACJ, Harren FJ, Bögemann GM, Blom CWPM, Reuss J (1990) Ethylene production and petiole growth in Rumex plants induced by soil waterlogging: the application of a continuous flow system and a laser driven intracavity photoacoustic detection system. Plant Physiology 94, 1071–1077.
Ethylene production and petiole growth in Rumex plants induced by soil waterlogging: the application of a continuous flow system and a laser driven intracavity photoacoustic detection system.Crossref | GoogleScholarGoogle Scholar |

Vogel KP, Moore KJ (1998) Forage yield and quality of tall wheatgrass accessions in the USDA Germplasm Collection. Crop Science 38, 509–512.
Forage yield and quality of tall wheatgrass accessions in the USDA Germplasm Collection.Crossref | GoogleScholarGoogle Scholar |