Functional Strategies and Life Histories of Grasses Underlying Yield and Resilience
Sharon Crowley
School of Biological, Earth & Environmental Sciences and Environmental Research Institute, University College Cork, Cork, Ireland
Search for more papers by this authorAstrid Wingler
School of Biological, Earth & Environmental Sciences and Environmental Research Institute, University College Cork, Cork, Ireland
Search for more papers by this authorSharon Crowley
School of Biological, Earth & Environmental Sciences and Environmental Research Institute, University College Cork, Cork, Ireland
Search for more papers by this authorAstrid Wingler
School of Biological, Earth & Environmental Sciences and Environmental Research Institute, University College Cork, Cork, Ireland
Search for more papers by this authorAbstract
The family of Poaceae (grasses) includes many economically important crops. While grass grain crops (cereals) are typically annual, bioenergy and forage crops can have annual or perennial life histories. Annuals and perennials differ in important life history traits, such as the regulation of flowering and senescence, which determine to what extent resources are allocated to the grain, vegetative growth, or storage. These differences are also reflected in physiological characteristics; in particular, leaf traits that can be used to determine functional strategies (competitive, stress tolerant, or ruderal). While ruderality is associated with yield in annual grain crops, stress tolerance is usually higher in perennials. In this article, we discuss variation in functional strategies within perennial ryegrass grass (Lolium perenne) and species of the genus Brachypodium, demonstrating variation in characteristics for ruderality and stress tolerance. We argue that regulation of senescence of organs and whole plants determines these strategies and propose ideas on how functional strategies could potentially be optimised to increase grain yield in perennial grasses while maintaining stress resilience and other beneficial traits associated with perenniality.
References
- Al-Beyroutiová, M., Sabo, M., Sleziak, P. et al. (2016). Evolutionary relationships in the genus Secale revealed by DArTseq DNA polymorphism. Plant Systematics and Evolution 302: 1083–1091.
- Atkinson, R.R.L., Mockford, E.J., Bennett, C. et al. (2016). C4 photosynthesis boosts growth by altering physiology, allocation and size. Nature Plants 2: 16038.
- Barbier, P., Morishima, H., and Ishihama, A. (1991). Phylogenetic relationships of annual and perennial wild rice: probing by direct DNA sequencing. Theoretical and Applied Genetics 81: 693–702.
- Baum, B.R., Edwards, T., and Johnson, D.A. (2013). What does the 5S rRNA multigene family tell us about the origin of the annual Triticeae (Poaceae)? Genome 56: 245–266.
- Bennett, E., Roberts, J.A., and Wagstaff, C. (2012). Manipulating resource allocation in plants. Journal of Experimental Botany 63 (9): 3391–3400.
- Bettgenhaeuser, J., Corke, F.M., Opanowicz, M. et al. (2017). Natural variation in Brachypodium links vernalization and flowering time loci as major flowering determinants. Plant Physiology 173 (1): 256–268.
- Boonman, A., Anten, N.P., Dueck, T.A. et al. (2006). Functional significance of shade-induced leaf senescence in dense canopies: an experimental test using transgenic tobacco. American Naturalist 168 (5): 597–607.
- Borrill, P., Fahy, B., Smith, A.M., and Uauy, C. (2015). Wheat grain filling is limited by grain filling capacity rather than the duration of flag leaf photosynthesis: a case study using NAM RNAi plants. PLoS One 10 (8): e0134947.
- Brutnell, T.P., Bennetzen, J.L., and Vogel, J.P. (2015). Brachypodium distachyon and Setaria viridis: model genetic systems for the grasses. Annual Review of Plant Biology 66: 465–485.
- Burnett, A.C., Rogers, A., Rees, M., and Osborne, C. (2016). Carbon source–sink limitations differ between two species with contrasting growth strategies. Plant, Cell and Environment 39 (11): 2460–2472.
- Campetella, G., Botta-Dukát, Z., Wellstein, C. et al. (2011). Patterns of plant trait–environment relationships along a forest succession chronosequence. Agriculture, Ecosystems & Environment 145 (1): 38–48.
- Catalán, P., Müller, J., Hasterok, R. et al. (2012). Evolution and taxonomic split of the model grass Brachypodium distachyon . Annals of Botany 109: 385–405.
- Catalán, P., Chalhoub, B., Chochois, V. et al. (2014). Update on the genomics and basic biology of Brachypodium: International Brachypodium Initiative (IBI). Trends in Plant Science 19 (7): 414–418.
- Catalán, P., López-Alvarez, D., Díaz-Pérez, A. et al. (2016). Phylogeny and evolution of the genus Brachypodium . In: Genetics and Genomics of Brachypodium. Plant Genetics and Genomics: Crops Models (ed. J.P. Vogel), 9–38. Switzerland: Springer.
- Cerabolini, B.E.L., Brusa, G., Ceriani, R.M. et al. (2010). Can CSR classification be generally applied outside Britain? Plant Ecology 210 (2): 253–261.
- Cox, S., Nabukalu, P., Paterson, A.H. et al. (2018). Development of perennial grain sorghum. Sustainability 10 (1): 172.
- Cui, L., Ren, Y., Murray, T.D. et al. (2018). Development of perennial wheat through hybridization between wheat and wheatgrasses: a review. Engineering 4 (4): 507–513.
- DeHaan, L., Christians, M., Crain, J., and Poland, J. (2018). Development and evolution of an intermediate wheatgrass domestication program. Sustainability 10 (5): 1499.
- Des Roches, S., Post, D.M., Turley, N.E. et al. (2018). The ecological importance of intraspecific variation. Nature Ecology & Evolution 2 (1): 57.
- Díaz-Pérez, A., López-Álvarez, D., Sancho, R., and Catalán, P. (2018). Reconstructing the origins and the biogeography of species' genomes in the highly reticulate allopolyploid-rich model grass genus Brachypodium using minimum evolution, coalescence and maximum likelihood approaches. Molecular Phylogenetics and Evolution 127: 256–271.
- Dillard, S.L., Hancock, D.W., Harmon, D.D. et al. (2018). Animal performance and environmental efficiency of cool- and warm-season annual grazing systems. Journal of Animal Science 96 (8): 3491–3502.
- Distelfeld, A., Avni, R., and Fischer, A.M. (2014). Senescence, nutrient remobilization, and yield in wheat and barley. Journal of Experimental Botany 65 (14): 3783–3798.
- Dohleman, F.G. and Long, S.P. (2009). More productive than maize in the Midwest: how does Miscanthus do it? Plant Physiology 150 (4): 2104–2115.
- D'Ottavio, P., Francioni, M., Trozzo et al. (2018). Trends and approaches in the analysis of ecosystem services provided by grazing systems: A review. Grass and Forage Science 73 (1): 15–25.
- Easlon, H.M., Nemali, K.S., Richards, J.H. et al. (2014). The physiological basis for genetic variation in water use efficiency and carbon isotope composition in Arabidopsis thaliana . Photosynthesis Research 119 (1-2): 119–129.
- Elberse, I.A.M., Vanhala, T.K., Turin, J.H.B. et al. (2004). Quantitative trait loci affecting growth-related traits in wild barley (Hordeum spontaneum) grown under different levels of nutrient supply. Heredity 93 (1): 22–33.
- El-Lithy, M.E., Clerkx, E.J.M., Ruys, G.J. et al. (2004). Quantitative trait locus analysis of growth-related traits in a new Arabidopsis recombinant inbred population. Plant Physiology 135 (1): 444–458.
- Garnier, E. (1992). Growth analysis of congeneric annual and perennial grass species. Journal of Ecology 80 (4): 665–675.
- Garnier, E. and Laurent, G. (1994). Leaf anatomy, specific mass and water content in congeneric annual and perennial grass species. New Phytologist 128 (4): 725–736.
- Garnier, E. and Vancaeyzeele, S. (1994). Carbon and nitrogen content of congeneric annual and perennial grass species: relationships with growth. Plant, Cell & Environment 17 (4): 399–407.
- Garnier, E., Laurent, G., Bellmann, A. et al. (2001). Consistency of species ranking based on functional leaf traits. New Phytologist 152 (1): 69–83.
- Garnier, E., Lavorel, S., Ansquer, P. et al. (2007). Assessing the effects of land-use change on plant traits, communities and ecosystem functioning in grasslands: a standardized methodology and lessons from an application to 11 European sites. Annals of Botany 99 (5): 967–985.
-
Gordon, S.P., Liu, L., and Vogel, J.P. (2015). The genus Brachypodium as a model for perenniality and polyploidy. In: Genetics and Genomics of Brachypodium, 313–325. Cham: Springer.
10.1007/7397_2015_19 Google Scholar
- Gregersen, P.L., Holm, P.B., and Krupinska, K. (2008). Leaf senescence and nutrient remobilisation in barley and wheat. Plant Biology 10 (s1): 37–49.
- Gregersen, P.L., Culetic, A., Boschian, L., and Krupinska, K. (2013). Plant senescence and crop productivity. Plant Molecular Biology 82 (6): 603–622.
- Grime, J.P. (1977). Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. American Naturalist 111 (982): 1169–1194.
-
Grime, J.P., Hodgson, J.G., and Hunt, R. (1988). Comparative Plant Ecology: A Functional Approach to Common British Species. The Netherlands: Springer.
10.1007/978-94-017-1094-7 Google Scholar
- Hæggström, C.A. and Skytén, R. (1996). Flowering and individual survival of a population of the grass Brachypodium sylvaticum in Nåtö, Åland Islands, SW Finland. Annales Botanici Fennici 33 (1): 1–10.
- Hennessy, D., O'Donovan, M., French, P., and Laidlaw, A.S. (2008). Factors influencing tissue turnover during winter in perennial ryegrass-dominated swards. Grass and Forage Science 63 (2): 202–211.
- Hodgson, J.G., Wilson, P.J., Hunt, R. et al. (1999). Allocating CSR plant functional types: a soft approach to a hard problem. Oikos 85 (2): 282–294.
- Hodkinson, T.R., Klaas, M., Jones, M.B. et al. (2015). Miscanthus: a case study for the utilization of natural genetic variation. Plant Genetic Resources 13 (3): 219–237.
- Hodkinson, T.R. (2018). Evolution and taxonomy of the grasses (Poaceae): a model family for the study of species-rich groups. Annual Plant Reviews 1: 1–39.
- Hu, F.Y., Tao, D.Y., Sacks, E. et al. (2003). Convergent evolution of perenniality in rice and sorghum. Proceedings of the National Academy of Sciences USA 100 (7): 4050–4054.
- Hyun, Y., Vincent, C., Tilmes, V. et al. (2019). A regulatory circuit conferring varied flowering response to cold in annual and perennial plants. Science 363 (6425): 409–412.
- Isbell, F., Craven, D., Connolly, J. et al. (2015). Biodiversity increases the resistance of ecosystem productivity to climate extremes. Nature 526: 574–577.
- Jakob, S.S., Meister, A., and Blattner, F.R. (2004). The considerable genome size variation of Hordeum species (Poaceae) is linked to phylogeny, life form, ecology, and speciation rates. Molecular Biology and Evolution 21 (5): 860–869.
- Jones, M.B., Finnan, J., and Hodkinson, T.R. (2015). Morphological and physiological traits for higher biomass production in perennial rhizomatous grasses grown on marginal land. Global Change Biology Bioenergy 7 (2): 375–385.
- Kantar, M.B., Tyl, C.E., Dorn, K.M. et al. (2016). Perennial grain and oilseed crops. Annual Review of Plant Biology 67: 703–729.
- Kattge, J., Díaz, S., Lavorel, S. et al. (2011). TRY – a global database of plant traits. Global Change Biology 17 (9): 2905–2935.
- Kellogg, E.A. (2015). Brachypodium distachyon as a genetic model system. Annual Reviews of Genetics 49: 1–20.
- Khan, M.A. and Stace, C.A. (1998). Breeding relationships in the genus Brachypodium (Poaceae: Pooideae). Nordic Journal of Botany 19 (3): 257–269.
- Kiefer, C., Severing, E., Karl, R. et al. (2017). Divergence of annual and perennial species in the Brassicaceae and the contribution of cis-acting variation at FLC orthologues. Molecular Ecology 26: 3437–3457.
- Kiefer, C., Bergonzi, S., Brand, L. et al. (2019). Contrasting life history traits in monocarpic versus polycarpic plants from a molecular-evolutionary point of view. Annual Plant Reviews 2: 1–25.
- Kleyer, M., Bekker, R.M., Knevel, I.C. et al. (2008). The LEDA Traitbase: a database of life-history traits of the Northwest European flora. Journal of Ecology 96 (6): 1266–1274.
- Lange, M., Eisenhauer, N., Sierra, C.A. et al. (2015). Plant diversity increases soil microbial activity and soil carbon storage. Nature Communications 6: 6707.
- Lauenroth, W.K. and Adler, P.B. (2008). Demography of perennial grassland plants: survival, life expectancy and life span. Journal of Ecology 96 (5): 1023–1032.
-
Lemaire, G., Hodgson, J., and Chabbi, A. (2011). Food security and environmental impacts – challenges for grassland sciences. In: Grassland Productivity and Ecosystem Services (eds. G. Lemaire, J. Hodgson and A. Chabbi), xii–xvii. Wallingford, UK: CAB International.
10.1079/9781845938093.A Google Scholar
- Li, C., Rudi, H., Stockinger, E.J. et al. (2012). Comparative analyses reveal potential uses of Brachypodium distachyon as a model for cold stress responses in temperate grasses. BMC Plant Biology 12 (1): 65.
- Li, Y. and Shipley, B. (2017). An experimental test of CSR theory using a globally calibrated ordination method. PLoS One 12 (4): e0175404.
- Liu, H., Taylor, S.H., Xu, Q. et al. (2019). Life history is a key factor explaining functional trait diversity among subtropical grasses, and its influence differs between C3 and C4 species. Journal of Experimental Botany 70 (5): 1567–1580.
- Lusinska, J., Majka, J., Betekhtin, A. et al. (2018). Chromosome identification and reconstruction of evolutionary rearrangements in Brachypodium distachyon, B. stacei and B. hybridum . Annals of Botany 122 (3): 445–459.
- May, R.L., Warner, S., and Wingler, A. (2017). Classification of intra-specific variation in plant functional strategies reveals adaptation to climate. Annals of Botany 119 (8): 1343–1352.
- Meilhac, J., Durand, J.-L., Beguier, V., and Litrico, I. (2019). Increasing the benefits of species diversity in multispecies temporary grasslands by increasing within-species diversity. Annals of Botany 123 (5): 891–900.
- Minasny, B., Malone, B.P., McBratney, A.B. et al. (2017). Soil carbon 4 per mille. Geoderma 292: 59–86.
- O'Hara, L.E., Paul, M.J., and Wingler, A. (2013). How do sugars regulate plant growth and development? New insight into the role of trehalose-6-phosphate. Molecular Plant 6 (2): 261–273.
- Onoda, Y., Wright, I.J., Evans, J.R. et al. (2017). Physiological and structural tradeoffs underlying the leaf economics spectrum. New Phytologist 214 (4): 1447–1463.
- Parrott, D.L., McInnerney, K., Feller, U., and Fischer, A.M. (2007). Steam-girdling of barley (Hordeum vulgare) leaves leads to carbohydrate accumulation and accelerated leaf senescence, facilitating transcriptomic analysis of senescence-associated genes. New Phytologist 176 (1): 56–69.
- Peñuelas, J. and Munné-Bosch, S. (2010). Potentially immortal? New Phytologist 187 (3): 564–567.
- Pierce, S., Ceriani, R.M., De Andreis, R. et al. (2007). The leaf economics spectrum of Poaceae reflects variation in survival strategies. Plant Biosystems 141 (3): 337–343.
- Pierce, S., Brusa, G., Vagge, I., and Cerabolini, B. (2013). Allocating CSR plant functional types: the use of leaf economics and size traits to classify woody and herbaceous vascular plants. Functional Ecology 27 (4): 1002–1010.
- Pierce, S., Bottinelli, A., Bassani, I. et al. (2014). How well do seed production traits correlate with leaf traits, whole-plant traits and plant ecological strategies? Plant Ecology 215 (11): 1351–1359.
- Pierce, S., Negreiros, D., Cerabolini, B.E. et al. (2017). A global method for calculating plant CSR ecological strategies applied across biomes world-wide. Functional Ecology 31 (2): 444–457.
- Sade, N., del Mar Rubio-Wilhelmi, M., Umnajkitikorn, K., and Blumwald, E. (2018). Stress-induced senescence and plant tolerance to abiotic stress. Journal of Experimental Botany 69 (4): 845–853.
- Sage, R.F., de Melo Peixoto, M., Friesen, P., and Deen, B. (2015). C4 bioenergy crops for cool climates, with special emphasis on perennial C4 grasses. Journal of Experimental Botany 66 (14): 4195–4212.
- Sánchez González, J.J., Ruiz Corral, J.A., Medina García, G. et al. (2018). Ecogeography of teosinte. PLoS One 13 (2): e0192676.
- Scholthof, K.-B.G., Irigoyen, S., Catalán, P., and Mandadi, K.K. (2018). Brachypodium: a monocot grass model genus for plant biology. Plant Cell 30 (8): 1673–1694.
- Schoppach, R., Taylor, J.D., Majerus, E. et al. (2016). High resolution mapping of traits related to whole-plant transpiration under increasing evaporative demand in wheat. Journal of Experimental Botany 67 (9): 2847–2860.
- Sharma, N., Ruelens, P., D'hauw, M. et al. (2017). A Flowering Locus C homolog is a vernalization-regulated repressor in Brachypodium and is cold regulated in wheat. Plant Physiology 173 (2): 1301–1315.
- Shipley, B., De Bello, F., Cornelissen, J.H.C. et al. (2016). Reinforcing loose foundation stones in trait-based plant ecology. Oecologia 180 (4): 923–931.
- Smaje, C. (2015). The strong perennial vision: a critical review. Agroecology and Sustainable Food Systems 39 (5): 471–499.
- Soussana, J.-F., Lutfalla, S., Ehrhardt, F. et al. (2019). Matching policy and science: Rationale for the ‘4 per 1000 – soils for food security and climate’ initiative. Soil & Tillage Research 188: 3–15.
- Steinwand, M.A., Young, H.A., Bragg, J.N. et al. (2013). Brachypodium sylvaticum, a model for perennial grasses: transformation and inbred line development. PLoS One 8 (9): e75180.
- Suttie, J.M., Reynolds, S.G., and Batello, C. (2005). Grasslands of the World. Plant Production and Protection Series No. 34. Rome: Food and Agriculture Organization of the United Nations.
- Thomas, H. and Ougham, H. (2014). The stay-green trait. Journal of Experimental Botany 65 (14): 3889–3900.
- Van Tassel, D.L., DeHaan, L.R., and Cox, T.S. (2010). Missing domesticated plant forms: can artificial selection fill the gap? Evolutionary Applications 3 (5–6): 434–452.
- Vasseur, F., Sartori, K., Baron, E. et al. (2018). Climate as a driver of adaptive variations in ecological strategies in Arabidopsis thaliana . Annals of Botany 122 (5): 935–945.
- Vico, G., Manzoni, S., Nkurunziza, L., and Murphy, K. (2016). Trade-offs between seed output and life span – a quantitative comparison of traits between annual and perennial congeneric species. New Phytologist 209 (1): 104–114.
- Volaire, F. and Norton, N. (2006). Summer dormancy in perennial temperate grasses. Annals of Botany 98 (5): 927–933.
- Wang, R., Farrona, S., Vincent, C. et al. (2009). PEP1 regulates perennial flowering in Arabis alpina . Nature 459 (7245): 423–427.
- Wang, J. and Forster, J.W. (2017). Flowering time regulation in perennial ryegrass. Euphytica 213: 106.
- Wilson, P.J., Thompson, K., and Hodgson, J.G. (1999). Specific leaf area and leaf dry matter content as alternative predictors of plant strategies. New Phytologist 143 (1): 155–162.
- Wingler, A. and Hennessy, D. (2016). Limitation of grassland productivity by low temperature and seasonality of growth. Frontiers in Plant Science 7: 1130.
- Wingler, A. (2018). Transitioning to the next phase: the role of sugar signaling throughout the plant life cycle. Plant Physiology 176 (2): 1075–1084.
- Woods, D.P., Bednarek, R., Bouché, F. et al. (2017). Genetic architecture of flowering-time variation in Brachypodium distachyon . Plant Physiology 173 (1): 269–279.
- Wright, I.J., Reich, P.B., Westoby, M. et al. (2004). The world-wide leaf economics spectrum. Nature 428 (6985): 821–827.
- Xu, S. and Chong, K. (2018). Remembering winter through vernalization. Nature Plants 4: 997–1009.
- Yang, D., Liu, Y., Cheng, H. et al. (2016a). Genetic dissection of flag leaf morphology in wheat (Triticum aestivum L.) under diverse water regimes. BMC Genetics 17: 94.
- Yang, J., Worley, E., Ma, Q. et al. (2016b). Nitrogen remobilization and conservation, and underlying senescence-associated gene expression in the perennial switchgrass Panicum virgatum . New Phytologist 211 (1): 75–89.
- Yang, J. and Udvardi, M. (2018). Senescence and nitrogen use efficiency in perennial grasses for forage and biofuel production. Journal of Experimental Botany 69 (4): 855–865.
- Zuloaga, F.O., Salariato, D.L., and Scataglini, A. (2018). Molecular phylogeny of Panicum s. str. (Poaceae, Panicoideae, Paniceae) and insights into its biogeography and evolution. PLoS One 13 (2): e0191529.
- Zwicke, M., Picon-Cochard, C., Morvan-Bertrand, A. et al. (2015). What functional strategies drive drought survival and recovery of perennial species from upland grassland? Annals of Botany 116: 1001–1015.
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