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Early Physiological Mechanisms of Weed Competition

Published online by Cambridge University Press:  20 January 2017

Maha Afifi  and
Clarence Swanton
Maha Afifi
Affiliation:
Department of Plant Agriculture, Crop Science Building, University of Guelph, 50 Stone Road E., Guelph, ON, N1G 2W1, Canada
Clarence Swanton*
Affiliation:
Department of Plant Agriculture, Crop Science Building, University of Guelph, 50 Stone Road E., Guelph, ON, N1G 2W1, Canada
*
Corresponding author's E-mail: cswanton@uoguelp.ca
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Abstract

Early physiological mechanisms that occur in crop plants in response to neighboring weeds are not well understood. In this experiment, it was hypothesized that, in the absence of direct competition for resources, low red to far red ratio (R:FR) reflected from neighboring weeds will modulate the phenylpropanoid pathway, increase hydrogen peroxide (H2O2), and up-regulate the expression of ethylene biosynthesis and auxin transport genes. Laboratory experiments were conducted under conditions of nonlimiting resources using perennial ryegrass as a model weed species. We discovered that the detection by phytochrome (Phy) of low R:FR signals reflected from both biological and nonbiological sources triggered an up-regulation of ethylene biosynthesis genes and stimulated an auxin transport gene. The low R:FR also modulated the phenylpropanoid pathway resulting in a reduction in anthocyanin content and an enhancement of lignin synthesis. The presence of neighboring weeds also caused an accumulation of H2O2 in the first leaf and crown root tissues of the maize seedling. Stomata were observed to be closed as H2O2 accumulated in leaf tissue. This is the first study to report the modulation of phenylpropanoid pathway and the accumulation of H2O2 attributed to low R:FR. We further suggest that these physiological changes that occur in response to early weed competition result in a physiological cost to the crop plant, which contributes to the rapid loss in yield observed in weed competition studies conducted under field conditions.

Keywords

MaizeZea mays L.perennial ryegrass, Lolium perenne L.red to far-redR:FRhydrogen peroxideH2O2Weed competitionphenylpropanoid pathwayanthocyaninligninfree radicalscrown roots
Type
Weed Biology and Ecology
Information
Weed Science , Volume 60 , Issue 4 , December 2012 , pp. 542 - 551
Copyright
Copyright © Weed Science Society of America 

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References

Literature Cited

Afifi, M. and Swanton, C. J. 2011. Maize seed and stem roots differ in response to neighbouring weeds. Weed Res. 51:442–450.Google Scholar
Ballaré, C. L. 2009. Illuminated behaviour: phytochrome as a key regulator of light forging and plant anti-herbivore defence. Plant Cell Environ. 32:713–725.Google Scholar
Besseau, S., Hoffman, L., Geoffroy, P., Lapierre, C., Pollet, B., and Legrand, M. 2007. Flavonoid accumulation in Arabidopsis repressed in lignin synthesis affects auxin transport and plant growth. Plant Cell. 19:148–162.Google Scholar
Bhalerao, R. P., Eklöf, J., Ljung, K., Marchant, A., Bennett, M., and Sandberg, G. 2002. Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings. Plant J. 29:325–332.Google Scholar
Boccalandro, H. E., Rugnone, M. L., Moreno, J. E., Ploschuk, E. L., Serna, L., Yanovsky, M. J., and Casal, J. J. 2009. Phytochrome B enhances photosynthesis at the expense of water-use efficiency in Arabidopsis . Plant Physiol. 150:1083–1092.Google Scholar
Bosnić, A. Č. and Swanton, C. J. 1997. Influence of barnyardgrass (Echinochloa crus-galli) time of emergence and density on corn (Zea mays). Weed Sci. 45:276–282.Google Scholar
Bruce, R. J. and West, C. A. 1989. Elicitation of lignin biosynthesis and isoperoxidase activity by pectic fragments in suspension cultures of castor bean. Plant Physiol. 91:889–897.Google Scholar
Cervantes, E. and Tocino, Á. 2009. Ethylene, free radicals and the transition between stable states in plant morphology. Plant Signal Behav. 5:367–371.Google Scholar
Dolan, L. 1997. The role of ethylene in the development of plant form. J. Exp. Bot. 48:201–210.Google Scholar
El-Kereamy, A., Chervin, C., Roustan, J. P., Cheynier, V., Souquet, J. M., Moutounet, M., Raynal, J., Ford, C., Latché, A., Pech, J. C., and Bouzayen, M. 2003. Exogenous ethylene stimulates the long-term expression of genes related to anthocyanin biosynthesis in grape berries. Physiol. Plant. 119:175–182.Google Scholar
Foyer, C. H. and Shigeoka, S. 2011. Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol. 155:93–100.Google Scholar
Gälweiler, L., Guan, C., Muller, A., Wisman, E., Mendgen, K., Yephremov, A., and Palme, K. 1998. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science. 282:2226–2230.Google Scholar
Gill, S. S. and Tuteja, N. 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48:909–930.Google Scholar
Gould, K. 2004. Nature's Swiss army knife: the diverse protective roles of anthocyanins in leaves. J. Biomed. Biotechnol. 5:314–320.Google Scholar
Harper, J. L., ed. 1977. Population Biology of Plants. 4th ed. New York Academic Press. 306 p.Google Scholar
Horvath, D. P., Gulden, R., and Clay, S. A. 2006. Microarray analysis of late season velvetleaf (Abutilon theophrasti) impact on corn. Weed Sci. 54:983–994.Google Scholar
Jiao, Y., Lau, O. S., and Deng, X. W. 2007. Light-regulated transcriptional networks in higher plants. Nature Rev. Genet. 8:217–230.Google Scholar
Jones, M. A., Raymond, M. J., Yang, Z., and Smirnoff, N. 2007. NADPH oxidase-dependent reactive oxygen species formation required for root hair growth depends on ROP GTPase. J. Exp. Bot. 58:1261–1270.Google Scholar
Joo, J. H., Bae, Y. S., and Lee, J. S. 2001. Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiol. 126:1055–1060.Google Scholar
Kasperbauer, M. J. and Karlen, D. L. 1994. Plant spacing and reflected far-red light effects on phytochrome-regulated photosynthate allocation in corn seedlings. Crop Sci. 34:1564–1569.Google Scholar
Kawasaki, T., Koita, H., Nakatsubo, T., Hasegawa, K., Wakabayashi, K., Takahashi, H., Umemura, K., Umezawa, T., and Shimamoto, K. 2006. Cinnamoyl-CoA reductase, a key enzyme in lignin biosynthesis, is an effector of small GTPase Rac in defense signaling in rice. PNAS. 103:230–235.Google Scholar
Keuskamp, D. H., Pollmannb, S., Voeseneka, L. A. C. J., Peetersa, A. J. M., and Pierik, R. 2010. Auxin transport through PIN-FORMED 3 (PIN3) controls shade avoidance and fitness during competition. PNAS. 107:22740–22744.Google Scholar
Knezevic, S. Z., Weise, S. F., and Swanton, C. J. 1994. Interference of redroot pigweed (Amaranthus retroflexus) in corn (Zea mays). Weed Sci. 42:568–573.Google Scholar
Kropff, M. J. and Spitters, C. J. T. 1991. A simple model of crop loss by weed competition from early observation on relative leaf area of the weeds. Weed Res. 31:97–105.Google Scholar
Livak, K. J. and Schmittgen, T. D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔC T method. Methods. 25:402–408.Google Scholar
Mittler, R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends in Plant Sci. 7:405–410.Google Scholar
Moriles, J. C., Hansen, S., Reicks, G., Horvath, D. P., Clay, D. E., and Clay, S. A. 2012. Microarray and growth analyses identify differences and similarities of early corn response to weeds, shade, and nitrogen stresses. Weed Sci. 60:158–166.Google Scholar
Neff, M. M. and Chory, J. 1998. Genetic interactions between phytochrome A, phytochrome B, and cryptochrome 1 during Arabidopsis development. Plant Physiol. 118:27–35.Google Scholar
Neuhaus, G., Bowler, C., Hiratsuka, K., Yamagata, H., and Chua, N. H. 1997. Phytochrome-regulated repression of gene expression requires calcium and cGMP. The EMBO J. 16:2554–2564.Google Scholar
Page, E. R., Tollenaar, M., Lee, E. A., Lukens, L., and Swanton, C. J. 2010. Shade avoidance: an integral component of crop weed competition. Weed Res. 50:281–288.Google Scholar
Pasternak, T., Rudas, V., Potters, G., and Jansen, M. A. K. 2005. Morphogenic effects of abiotic stress: reorientation of growth in Arabidopsis thaliana seedlings. Environ. Exp. Bot. 53:299–314.Google Scholar
Patterson, B. D., Macrae, E. A., and Ferguson, I. B. 1984. Estimation of hydrogen peroxide in plant extracts using titanium (IV). Anal. Biochem. 139:487–492.Google Scholar
Peng, M., Hudson, D., Schofield, A., Tsao, R., Yang, R., Gu, H., Bi, Y. M., and Rothstein, S. J. 2008. Adaptation of Arabidopsis to nitrogen limitation involves induction of anthocyanin synthesis which is controlled by the NLA gene. J. Exp. Bot. 59:2933–2944.Google Scholar
Pierik, R., Cuppens, M. L. C., Voesenek, L. A. C. J., and Visser, E. J. W. 2004a. Interaction between ethylene and gibberellins in phytochrome-mediated shade avoidance responses in Tobacco. Plant Physiol. 136:2928–2936.Google Scholar
Pierik, R., Whitelam, G. C., Voesenek, L. A. C. J., De Kroon, H., and Visser, E. J. W. 2004b. Canopy studies on ethylene-insensitive tobacco identify ethylene as a novel element in blue light and plant-plant signalling. Plant J. 38:310–319.Google Scholar
Rabino, I., Mancinelli, A. L., and Kuzmanoff, K. M. 1977. Photocontrol of anthocyanin synthesis. VI. Spectral sensitivity, irradiance dependence, and reciprocity relationships. Plant Physiol. 59:569–573.Google Scholar
Rajcan, I., Chandler, K. J., and Swanton, C. J. 2004. Red-far-red ratio of reflected light: a hypothesis of why early season weed control is important in corn. Weed Sci. 52:774–778.Google Scholar
Rajcan, I. and Swanton, C. J. 2001. Understanding maize-weed competition: resource competition, light quality and the whole plant. Field Crop Res. 71:139–150.Google Scholar
Roth-Bejerano, N. and Itai, C. 1981. Involvement of phytochrome in stomatal movement: effect of blue and red light. Physiol. Plant. 52:201–206.Google Scholar
Ruzicka, K., Ljung, K., Vanneste, S., Podhorska, R., Beeckman, T., Friml, J., and Benkova, E. 2007. Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell. 19:2197–2212.Google Scholar
Smith, H. 1982. Light quality, photoperception, and plant strategy. Annu. Rev. Plant Physiol. 33:481–518.Google Scholar
Smith, H. and Holmes, M. G. 1977. The function of phytochrome in the natural environment. III. Measurement and calculation of phytochrome photoequilibrium. Photochem. PhotoBiol. 25:547–550.Google Scholar
Talbott, L. D., Zhu, J., Han, S. W., and Zeiger, E. 2002. Phytochrome and blue light-mediated stomatal opening in the orchid, Paphiopedilum . Plant Cell Physiol. 43:639–646.Google Scholar
Tao, Y., Ferrer, J. L., Ljung, K., Pojer, F., Hong, F., Long, J. A., Li, L., Moreno, J. E., Bowman, M. E., Ivans, L. J., Cheng, Y., Lim, J., Zhao, Y., Ballaré, C. L., Sandberg, G., Noel, J. P., and Chory, J. 2008. Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell. 133:164–176.Google Scholar
Thordal-Christensen, H., Zhang, Z., Wei, Y., and Collinge, D. B. 1997. Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 11:1187–1194.Google Scholar
Voleníková, M. and Tichá, I. 2001. Insertion profiles in stomatal density and sizes in Nicotiana tabacum L. plantlets. Biol. Plant. 44:161–165.Google Scholar
Wang, J. G., Chen, C. H., Chien, C. T., and Hsieh, H. L. 2011. Far-red insensitive 219 modulates constitutive phytomorphogenic1 activity via physical interaction to regulate hypocotyl elongation in Arabidopsis . Plant Physiol. 156:631–646.Google Scholar
Wang, K. L. C., Li, H., and Ecker, J. R. 2002. Ethylene biosynthesis and signalling networks. Plant Cell. 14:S131–S151.Google Scholar
Warnasooriya, S. N., Porter, K. J., and Montgomery, B. L. 2011. Tissue- and isoform-specific phytochrome regulation of light-dependent anthocyanin accumulation in Arabidopsis thaliana . Plant Signal Behav. 6:624–631.Google Scholar
Xiao, Z., Miao, Y. C., An, G. Y., Zhou, Y., Shangguan, Z. P., Gao, J. F., and Song, C. P. 2001. K+ channels inhibited by hydrogen peroxide mediate abscisic acid signaling in Vicia guard cells. Cell Res. 11:195–202.Google Scholar
Zhou, Y. and Singh, B. R. 2002. Red light stimulates flowering and anthocyanin biosynthesis in American cranberry. Plant Growth Regul. 38:165–171.Google Scholar