Hostname: page-component-7c8c6479df-fqc5m Total loading time: 0 Render date: 2024-03-28T13:50:57.270Z Has data issue: false hasContentIssue false

Experimental Methods for Estimation of Plant Fitness Costs Associated with Herbicide-Resistance Genes

Published online by Cambridge University Press:  20 January 2017

Martin M. Vila-Aiub
Affiliation:
Consejo Nacional de Investigaciones Científicas y Técnicas (IFEVA-CONICET), Facultad de Agronomía Universidad de Buenos Aires (UBA), Av. San Martin 4453, Buenos Aires (C1417DSE), Argentina
Pedro E. Gundel
Affiliation:
Consejo Nacional de Investigaciones Científicas y Técnicas (IFEVA-CONICET), Facultad de Agronomía Universidad de Buenos Aires (UBA), Av. San Martin 4453, Buenos Aires (C1417DSE), Argentina
Christopher Preston
Affiliation:
School of Agriculture, Food and Wine, University of Adelaide, PMB 1, Glen Osmond SA 5064, Australia
Rights & Permissions [Opens in a new window]

Extract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Since the beginning of agriculture, crops have been exposed to recurrent invasion by weeds that can impose severe reductions in crop quality and yield. There have been continuing efforts to reduce the impacts of weeds on production. More than 40 yr ago, overreliance on herbicide technology to reduce weed infestations resulted in the selection of adaptive traits that enabled weed survival and reproduction under herbicide treatments (Délye et al. 2007; Powles and Yu 2010; Vila-Aiub et al. 2008). As a result, herbicide resistance in > 200 weed species has evolved worldwide (Heap 2013; Powles 2008).

Type
Weed Biology and Ecology
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution license (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.
Copyright
Copyright © Weed Science Society of America

References

Literature Cited

Ashigh, J, Tardif, F (2007) An Ala205Val substitution in acetohydroxyacid synthase of Eastern black nightshade (Solanum ptychanthum) reduces sensitivity to herbicides and feedback inhibition. Weed Sci 55:558565Google Scholar
Ashigh, J, Tardif, FJ (2009) An amino acid substitution at position 205 of acetohydroxyacid synthase reduces fitness under optimal light in resistant populations of Solanum ptychanthum. Weed Res 49:47948910.1111/j.1365-3180.2009.00717.xGoogle Scholar
Baucom, RS, Mauricio, R (2004) Fitness costs and benefits of novel herbicide tolerance in a noxious weed. Proc Natl Acad Sci U S A 101:1338613390Google Scholar
Beckie, HJ, Heap, IM, Smeda, RJ, Hall, LM (2000) Screening for herbicide resistance in weeds. Weed Technol 14:428445Google Scholar
Bergelson, J, Purrington, CB (1996) Surveying patterns in the cost of resistance in plants. Am Nat 148:53655810.1086/285938Google Scholar
Busi, R, Neve, P, Powles, S (2013) Evolved polygenic herbicide resistance in Lolium rigidum by low-dose herbicide selection within standing genetic variation. Evol Appl 6:231242Google Scholar
Chang, SM, Rausher, MD (1998) Frequency-dependent pollen discounting contributes to maintenance of a mixed mating system in the common morning glory Ipomoea purpurea. Am Nat 152:67168310.1086/286198Google Scholar
Chapin, FS III, Autumn, K, Pugnaire, F (1993) Evolution of suites of traits in response to environmental-stress. Am Nat 142:S78S9210.1086/285524Google Scholar
Chauhan, BS, Gill, G, Preston, C (2006) Influence of tillage systems on vertical distribution, seedling recruitment and persistence of rigid ryegrass (Lolium rigidum) seed bank. Weed Sci 54:669676Google Scholar
Cocker, KM, Moss, SR, Coleman, J. O. D. (1999) Multiple mechanisms of resistance to fenoxaprop-P-ethyl in United Kingdom and other European populations of herbicide-resistant Alopecurus myosuroides (black-grass). Pestic Biochem Physiol 65:169180Google Scholar
Cockerton, H (2013) Investigating the Cost of Adaptation in Amaranthus tuberculatus Populations with Evolved Resistance to Glyphosate. Ph.D Dissertation. Coventry, UKUniversity of Warwick. 261 pGoogle Scholar
Cousens, RD, Gill, GS, Speijers, EJ (1997) Comment: number of sample populations required to determine the effects of herbicide resistance on plant growth and fitness. Weed Res 37:14Google Scholar
Crawley, M (1997) Plant Ecology. Hoboken, NJWiley-Blackwell. 510 pGoogle Scholar
Dasgupta, K, Ganesan, S, Manivasagam, S, Ayre, BG (2011) A cytochrome P450 mono-oxygenase commonly used for negative selection in transgenic plants causes growth anomalies by disrupting brassinosteroid signaling. BMC Plant Biol 11:67Google Scholar
Delph, LF, Weinig, C, Sullivan, K (1998) Why fast-growing pollen tubes give rise to vigorous progeny: the test of a new mechanism. Proc R Soc Lond B Biol Sci 265:93593910.1098/rspb.1998.0381Google Scholar
Délye, C (2005) Weed resistance to acetyl coenzyme A carboxylase inhibitors: an update. Weed Sci 53:728746Google Scholar
Délye, C, Jasieniuk, M, Le Corre, V (2013) Deciphering the evolution of herbicide resistance in weeds. Trends Genet 29:649658Google Scholar
Délye, C, Menchari, Y, Guillemin, JP, Matejicek, A, Michel, S, Camilleri, C, Chauvel, B (2007) Status of black grass (Alopecurus myosuroides) resistance to acetyl-coenzyme A carboxylase inhibitors in France. Weed Res 47:95105Google Scholar
Délye, C, Menchari, Y, Michel, S, Cadet, É, Le Corre, V (2013) A new insight into arable weed adaptive evolution: mutations endowing herbicide resistance also affect germination dynamics and seedling emergence. Ann Botany (Lond) 111:68169110.1093/aob/mct018Google Scholar
Dinelli, G, Marotti, I, Bonetti, A, Minelli, M, Catizone, P, Barnes, J (2006) Physiological and molecular insight on the mechanisms of resistance to glyphosate in Conyza canadensis (L.) Cronq. biotypes. Pestic Biochem Physiol 86:3041Google Scholar
Dyer, WE, Chee, PW, Fay, PK (1993) Rapid germination of sulfonylurea-resistant Kochia scoparia l accessions is associated with elevated seed levels of branched-chain amino-acids. Weed Sci 41:1822Google Scholar
Falconer, DS, Mackay, TFS (1996) Introduction to Quantitative Genetics. 4th edn. Essex, UKLongman. 480 pGoogle Scholar
Futuyma, DJ (2013) Evolution. Sunderland, MASinauer. 656 pGoogle Scholar
Gaines, TA, Zhang, W, Wang, D, Bukun, B, Chisholm, ST, Shaner, DL, Nissen, SJ, Patzoldt, WL, Tranel, PJ, Culpepper, AS, Grey, TL, Webster, TM, Vencill, WK, Sammons, RD, Jiang, J, Preston, C, Leach, JE, Westra, P (2010) Gene amplification confers glyphosate resistance in Amaranthus palmeri. Proc Natl Acad Sci U S A 107:1029103410.1073/pnas.0906649107Google Scholar
Gassmann, AJ (2005) Resistance to herbicide and susceptibility to herbivores: environmental variation in the magnitude of an ecological trade-off. Oecologia 145:57558510.1007/s00442-005-0112-6Google Scholar
Gassmann, AJ, Futuyma, DJ (2005) Consequence of herbivory for the fitness cost of herbicide resistance: photosynthetic variation in the context of plant-herbivore interactions. J Evol Biol 18:447454Google Scholar
Ge, X, d'Avignon, DA, Ackerman, JJH, Collavo, A, Sattin, M, Ostrander, EL, Hall, EL, Sammons, RD, Preston, C (2012) Vacuolar glyphosate-sequestration correlates with glyphosate resistance in ryegrass (Lolium spp.) from Australia, South America, and Europe: a 31P NMR investigation. J Agric Food Chem 60:12431250Google Scholar
Ge, X, d'Avignon, DA, Ackerman, JJH, Sammons, RD (2010) Rapid vacuolar sequestration: the horseweed glyphosate resistance mechanism. Pest Manag Sci 66:345348Google Scholar
Giacomini, D, Westra, P, Ward, SM (2014) Impact of genetic background in fitness cost studies: an example from glyphosate-resistant Palmer amaranth. Weed Sci 62:2937Google Scholar
Gillespie, JH (1998) Population Genetics: A Concise Guide. Baltimore, MDJohns Hopkins University PressGoogle Scholar
Gómez, JM (2004) Bigger is not always better: conflicting selective pressures on seed size in Quercus ilex. Evolution 58:718010.1111/j.0014-3820.2004.tb01574.xGoogle Scholar
Gressel, J, Bensinai, G (1985) Low intraspecific competitive fitness in a triazine-resistant, nearly nuclear-isogenic line of Brassica napus. Plant Sci 38:2932Google Scholar
Gressel, J, Segel, LA (1990) Modeling the effectiveness of herbicide rotations and mixtures as strategies to delay or preclude resistance. Weed Technol 4:186198Google Scholar
Grime, JP (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111:11691194Google Scholar
Gundel, P, Martinez-Ghersa, MA, Ghersa, CM (2008) Dormancy, germination, and ageing of Lolium multiflorum seeds following contrasting herbicide selection regimes. Eur J Agron 28:606613Google Scholar
Harder, LD, Wilson, WG (1998) A clarification of pollen discounting and its joint effects with inbreeding depression on mating system evolution. Am Nat 152:68469510.1086/286199Google Scholar
Hardstone, MC, Lazzaro, BP, Scott, JG (2009) The effect of three environmental conditions on the fitness of cytochrome P450 monooxygenase-mediated permethrin resistance in Culex pipiens quinquefasciatus. BMC Evol Biol 9:42Google Scholar
Harper, J (1977) Population Biology of Plants. LondonAcademicGoogle Scholar
Hart, J, Radosevich, S, Stemler, A (1992) Influence of light intensity on growth of triazine-resistant rapeseed (Brassica napus). Weed Res 32:34935610.1111/j.1365-3180.1992.tb01895.xGoogle Scholar
Heap, I (2013) The International Survey of Herbicide Resistant Weeds. http://www.weedscience.com. Accessed May 2 2013Google Scholar
Herms, DA, Mattson, WJ (1992) The dilemma of plants—to grow or defend. Q Rev Biol 67:28333510.1086/417659Google Scholar
Holt, JS, Thill, DC (1994) Growth and productivity of resistant plants. Pages 299316in Powles, SB, Holtum, JAM, eds. Herbicide Resistance in Plants: Biology and Biochemistry. Boca Raton, FLLewisGoogle Scholar
Jakobsson, A, Eriksson, O (2000) A comparative study of seed number, seed size, seedling size and recruitment in grassland plants. Oikos 88:49450210.1034/j.1600-0706.2000.880304.xGoogle Scholar
Jasieniuk, M, Brûlé-Babel, AL, Morrison, IN (1996) The evolution and genetics of herbicide resistance in weeds. Weed Sci 44:17619310.1017/S0043174500093747Google Scholar
Jordan, N (1999) Fitness effects of the triazine resistance mutation in Amaranthus hybridus: relative fitness in maize and soyabean crops. Weed Res 39:493505Google Scholar
Jurado, E, Westoby, M (1992) Seedling growth in relation to seed size among species of arid Australia. J Ecol 80:407416Google Scholar
Maxwell, B, Mortimer, A (1994) Selection for herbicide resistance. Pages 125in Powles, SB, Holtum, JAM, eds. Herbicide Resistance in Plants: Biology and Biochemistry. Boca Raton, FLLewisGoogle Scholar
Menchari, Y, Chauvel, B, Darmency, H, Delye, C (2008) Fitness costs associated with three mutant acetyl-coenzyme A carboxylase alleles endowing herbicide resistance in black-grass Alopecurus myosuroides. J Appl Ecol 45:939947Google Scholar
Mills, SK, Beatty, JH (1979) The propensity interpretation of fitness. Philos Sci 46:26328610.1086/288865Google Scholar
Nandula, VK, Reddy, KN, Poston, DH, Rimando, AM, Duke, SO (2008) Glyphosate tolerance mechanism in Italian ryegrass (Lolium multiflorum) from Mississippi. Weed Sci 56:344349Google Scholar
Orr, HA (2009) Fitness and its role in evolutionary genetics. Nat Rev Genet 10:53153910.1038/nrg2603Google Scholar
Owen, M, Michael, PJ, Renton, M, Steadman, KJ, Powles, SB (2011) Towards large-scale prediction of Lolium rigidum emergence, II: correlation between dormancy and herbicide resistance levels suggests an impact of cropping systems. Weed Res 51:133141Google Scholar
Paris, M, Roux, F, Berard, A, Reboud, X (2008) The effects of the genetic background on herbicide resistance fitness cost and its associated dominance in Arabidopsis thaliana. Heredity 101:499506Google Scholar
Pedersen, BP, Neve, P, Andreasen, C, Powles, SB (2007) Ecological fitness of a glyphosate-resistant Lolium rigidum population: growth and seed production along a competition gradient. Basic Appl Ecol 8:258268Google Scholar
Powles, SB (2008) Evolution in action: glyphosate-resistant weeds threaten world crops. Outlooks Pest Manag 19:256259Google Scholar
Powles, SB, Holtum, JAM (1994) Herbicide Resistance in Plants: Biology and Biochemistry. Boca Raton, FLLewis. 353 pGoogle Scholar
Powles, SB, Yu, Q (2010) Evolution in action: plants resistant to herbicides. Annu Rev Plant Biol 61:317347Google Scholar
Preston, C, Powles, SB (2002) Evolution of herbicide resistance in weeds: initial frequency of target site-based resistance to acetolactate synthase-inhibiting herbicides in Lolium rigidum. Heredity 88:81310.1038/sj.hdy.6800004Google Scholar
Preston, C, Stone, LM, Rieger, MA, Baker, J (2006) Multiple effects of a naturally occurring proline to threonine substitution within acetolactate synthase in two herbicide-resistant populations of Lactuca serriola. Pestic Biochem Physiol 84:227235Google Scholar
Preston, C, Tardif, FJ, Christopher, JT, Powles, SB (1996) Multiple resistance to dissimilar herbicide chemistries in a biotype of Lolium rigidum due to enhanced activity of several herbicide degrading enzymes. Pestic Biochem Physiol 54:123134Google Scholar
Preston, C, Wakelin, AM (2008) Resistance to glyphosate from altered herbicide translocation patterns. Pest Manag Sci 64:372376Google Scholar
Preston, C, Wakelin, AM, Dolman, FC, Bostamam, Y, Boutsalis, P (2009) A decade of glyphosate-resistant Lolium around the world: mechanisms, genes, fitness, and agronomic management. Weed Sci 57:435441Google Scholar
Primack, RB, Hyesoon, K (1989) Measuring fitness and natural selection in wild plant populations. Annu Rev Ecol Syst 20:367396Google Scholar
Purba, E, Preston, C, Powles, SB (1996) Growth and competitiveness of paraquat-resistant and -susceptible biotypes of Hordeum leporinum. Weed Res 36:311317Google Scholar
Purrington, CB (2000) Costs of resistance. Curr Opin Plant Biol 3:305308Google Scholar
Purrington, CB, Bergelson, J (1999) Exploring the physiological basis of costs of herbicide resistance in Arabidopsis thaliana. Am Nat 154:S82S9110.1086/303285Google Scholar
Reade, JPH, Milner, LJ, Cobb, AH (2004) A role for glutathione S-transferases in resistance to herbicides in grasses. Weed Sci 52:468474Google Scholar
Reader, R (1993) Control of seedling emergence by ground cover and seed predation in relation to seed size for some old-field species. J Ecol 169175Google Scholar
Ribeiro, DN, Pan, Z, Duke, SO, Nandula, VK, Baldwin, BS, Shaw, DR, Dayan, FE (2013) Involvement of facultative apomixis in inheritance of EPSPS gene amplification in glyphosate-resistant Amaranthus palmeri. Planta 114Google Scholar
Roff, DA (2002) Life History Evolution. Sunderland, MASinauer. 465 pGoogle Scholar
Roux, F, Camilleri, C, Bérard, A, Reboud, X (2005) Multigenerational versus single generation studies to estimate herbicide resistance fitness cost in Arabidopsis thaliana. Evolution 59:22642269Google Scholar
Roux, F, Gasquez, J, Reboud, X (2004) The dominance of the herbicide resistance cost in several Arabidopsis thaliana mutant lines. Genetics 166:44946010.1534/genetics.166.1.449Google Scholar
Roux, F, Giancola, S, Durand, S, Reboud, X (2006) Building of an experimental cline with Arabidopsis thaliana to estimate herbicide fitness cost. Genetics 173:1023103110.1534/genetics.104.036541Google Scholar
Roux, F, Reboud, X (2005) Is the cost of herbicide resistance expressed in the breakdown of the relationships between characters? a case study using synthetic-auxin-resistant Arabidopsis thaliana mutants. Genet Res 85:101110Google Scholar
Salzmann, D, Handley, RJ, Mueller-Scharer, H (2008) Functional significance of triazine-herbicide resistance in defence of Senecio vulgaris against a rust fungus. Basic Appl Ecol 9:57758710.1016/j.baae.2007.10.001Google Scholar
Sammons, D, Duncan, B, Wang, D, Ostrander, E, Rodriguez, C, Ge, X, d'Avignon, A, Ackerman, J (2010) Characterizing the glyphosate resistance mechanism in Johnsongrass. In: Working Landscapes Providing for the Future Weed Science Society of America Annual Meeting, Denver, CO. Champaign, ILWSSAGoogle Scholar
Scott, T, Rasgon, J, Black, W, Gould, F (2006) Fitness studies: developing a consensus methodology. Pages 171181in Knols, BGJ, Louis, C, eds. Bridging Laboratory and Field Research for Genetic Control of Disease Vectors. Wageningen, the NetherlandsSpringer/UR Frontis Series Volume 11Google Scholar
Siminszky, B (2006) Plant cytochrome P450-mediated herbicide metabolism. Phytochem Rev 5:44545810.1007/s11101-006-9011-7Google Scholar
Simms, EL, Rausher, MD (1987) Costs and benefits of plant-resistance to herbivory. Am Nat 130:570581Google Scholar
Song, Z, Lu, B, Zhu, Y, Chen, J (2002) Pollen competition between cultivated and wild rice species (Oryza sativa and O. rufipogon). New Phytol 153:289296Google Scholar
Stearns, SC (1989) Trade-offs in life-history evolution. Funct Ecol 3:259268Google Scholar
Strauss, SY, Rudgers, JA, Lau, JA, Irwin, RE (2002) Direct and ecological costs of resistance to herbivory. Trends Ecol Evol 17:278285Google Scholar
Tardif, FJ, Powles, SB (1994) Herbicide multiple-resistance in a Lolium rigidum biotype is endowed by multiple mechanisms—isolation of a subset with resistant acetyl-CoA carboxylase. Physiol Plant 91:488494Google Scholar
Tardif, FJ, Rajcan, I, Costea, M (2006) A mutation in the herbicide target site acetohydroxyacid synthase produces morphological and structural alterations and reduces fitness in Amaranthus powellii. New Phytol 169:251264Google Scholar
Tranel, PJ, Wright, TR (2002) Resistance of weeds to ALS-inhibiting herbicides: what have we learned? Weed Sci 50:700712Google Scholar
Uyenoyama, M (1986) Pleiotropy and the evolution of genetic systems conferring resistance to pesticides. Pages 207221in Glass, E, ed. Pesticide Resistance: Strategies and Tactics for Management. Washington, DCNational Academy of SciencesGoogle Scholar
Vila-Aiub, MM, Balbi, MC, Distéfano, AJ, Fernandez, L, Hopp, E, Yu, Q, Powles, SB (2012) Glyphosate resistance in perennial Sorghum halepense (Johnsongrass) endowed by reduced glyphosate translocation and leaf uptake. Pest Manag Sci 68:430436Google Scholar
Vila-Aiub, MM, Goh, SS, Gaines, TA, Han, H, Busi, R, Yu, Q, Powles, SB (2014) No fitness cost of glyphosate resistance endowed by massive EPSPS gene amplification in Amaranthus palmeri. Planta 239:79380110.1007/s00425-013-2022-xGoogle Scholar
Vila-Aiub, MM, Neve, P, Powles, SB (2005a) Resistance cost of a cytochrome P450 herbicide metabolism mechanism but not an ACCase target site mutation in a multiple resistant Lolium rigidum population. New Phytol 167:787796Google Scholar
Vila-Aiub, MM, Neve, P, Powles, SB (2009a) Evidence for an ecological cost of enhanced herbicide metabolism in Lolium rigidum. J Ecol 97:77278010.1111/j.1365-2745.2009.01511.xGoogle Scholar
Vila-Aiub, MM, Neve, P, Powles, SB (2009b) Fitness costs associated with evolved herbicide resistance alleles in plants. New Phytol 184:751767Google Scholar
Vila-Aiub, MM, Neve, P, Roux, F (2011) A unified approach to the estimation and interpretation of resistance costs in plants. Heredity 107:38639410.1038/hdy.2011.29Google Scholar
Vila-Aiub, MM, Neve, P, Steadman, KJ, Powles, SB (2005b) Ecological fitness of a multiple herbicide-resistant Lolium rigidum population: dynamics of seed germination and seedling emergence of resistant and susceptible phenotypes. J Appl Ecol 42:288298Google Scholar
Vila-Aiub, MM, Vidal, RA, Balbi, MC, Gundel, PE, Trucco, F, Ghersa, CM (2008) Glyphosate-resistant weeds of South American cropping systems: an overview. Pest Manag Sci 64:366371Google Scholar
Wakelin, AM, Lorraine-Colwill, DF, Preston, C (2004) Glyphosate resistance in four different populations of Lolium rigidum is associated with reduced translocation of glyphosate to meristematic zones. Weed Res 44:453459Google Scholar
Wakelin, AM, Preston, C (2006) A target-site mutation is present in a glyphosate-resistant Lolium rigidum population. Weed Res 46:432440Google Scholar
Wang, T, Picard, JC, Tian, X, Darmency, H (2010) A herbicide-resistant ACCase 1781 Setaria mutant shows higher fitness than wild type. Heredity 105:394400Google Scholar
Wang, W, Xia, H, Yang, X, Xu, T, Si, HJ, Cai, XX, Wang, F, Su, J, Snow, AA, Lu, B-R (2013) A novel 5-enolpyruvoylshikimate-3-phosphate (EPSP) synthase transgene for glyphosate resistance stimulates growth and fecundity in weedy rice (Oryza sativa) without herbicide. New Phytol. 202:679688 DOI:10.1111/nph.12428Google Scholar
Weiner, J (1990) Asymmetric competition in plant populations. Trends Ecol Evol 5:360364Google Scholar
Weiner, J, Campbell, LG, Pino, J, Echarte, L (2009) The allometry of reproduction within plant populations. J. Ecol. 97:1220–33Google Scholar
Weiner, J, Thomas, SC (1986) Size variability and competition in plant monocultures. Oikos 47:211222Google Scholar
Westoby, M, Leishman, M, Lord, J (1996) Comparative ecology of seed size and dispersal. Philos Trans R Soc Lond B Biol Sci 351:13091317Google Scholar
Williams, MMI, Jordan, N, Yerkes, C (1995) The fitness cost of triazine resistance in jimsonweed (Datura stramonium L.). Am Midl Nat 133:131137Google Scholar
Wright, S (1931) Evolution in Mendelian populations. Genetics 16:97159Google Scholar
Yu, Q, Ahmad-Hamdani, M, Han, H, Christoffers, M, Powles, S (2012) Herbicide resistance-endowing ACCase gene mutations in hexaploid wild oat (Avena fatua): insights into resistance evolution in a hexaploid species. Heredity 110:22023110.1038/hdy.2012.69Google Scholar
Yu, Q, Collavo, A, Zheng, MQ, Owen, M, Sattin, M, Powles, SB (2007) Diversity of acetyl-coenzyme a carboxylase mutations in resistant Lolium populations: evaluation using clethodim. Plant Physiol 145:547558Google Scholar
Yu, Q, Han, H, Vila-Aiub, MM, Powles, SB (2010) AHAS herbicide resistance endowing mutations: effect on AHAS functionality and plant growth. J Exp Bot 61:3925393410.1093/jxb/erq205Google Scholar