Photosynthetic response dynamics in the invasive species Tithonia diversifolia and two co-occurring native shrub species under fluctuating light conditions

doi:10.1016/j.pld.2023.04.001

Abstract

Abstract: To determine the invasiveness of invasive plants, many studies have compared photosynthetic traits or strategies between invasive and native species. However, few studies have compared the photosynthetic dynamics between invasive and native species during light fluctuations. We compared photosynthetic induction, relaxation dynamics and leaf traits between the invasive species, Tithonia diversifolia and two native species, Clerodendrum bungei and Blumea balsamifera, in full-sun and shady habitats. The photosynthetic dynamics and leaf traits differed among species. T. diversifolia showed a slower induction speed and stomatal opening response but had higher average intrinsic water-use efficiency than the two native species in full-sun habitats. Thus, the slow induction response may be attributed to the longer stomatal length in T. diversifolia. Habitat had a significant effect on photosynthetic dynamics in T. diversifolia and B. balsamifera but not in C. bungei. In shady habitat, T. diversifolia had a faster photosynthetic induction response than in full-sun habitat, leading to a higher average stomatal conductance during photosynthetic induction in T. diversifolia than in the two native species. In contrast, B. balsamifera had a larger stomatal length and slower photosynthetic induction and relaxation response in shady habitat than in full-sun habitat, resulting in higher carbon gain during photosynthetic relaxation. Nevertheless, in both habitats, T. diversifolia had an overall higher carbon gain during light fluctuations than the two native species. Our results indicated that T. diversifolia can adopt more effective response strategies under fluctuating light environments to maximize carbon gain, which may contribute to its successful invasion.

Key words: Invasive plant, Photosynthetic induction, Photosynthetic relaxation, Carbon gain, Stomatal traits, Tithonia diversifolia

Ju Li, Shu-Bin Zhang, Yang-Ping Li. Photosynthetic response dynamics in the invasive species Tithonia diversifolia and two co-occurring native shrub species under fluctuating light conditions[J]. Plant Diversity, 2024, 46(02): 265-273.

References

[1] Dai, G.H., Wang, S., Geng, Y.P., et al., 2021. Potential risks of Tithonia diversifolia in Yunnan Province under climate change. Ecol. Res. 36, 129-144.
[2] Deans, R.M., Brodribb, T.J., Busch, F.A., et al., 2019. Plant water-use strategy mediates stomatal effects on the light induction of photosynthesis. New Phytol. 222, 382-395.
[3] Diagne, C., Leroy, B., Vaissiere, A.C., et al., 2021. High and rising economic costs of biological invasions worldwide. Nature 592, 571-576.
[4] Drake, P.L., Froend, R.H., Franks, P.J., 2013. Smaller, faster stomata:scaling of stomatal size, rate of response, and stomatal conductance. J. Exp. Bot. 64, 495-505.
[5] Elliott-Kingston, C., Haworth, M., Yearsley, J.M., et al., 2016. Does size matter? Atmospheric CO2 may Be a stronger driver of stomatal closing rate than stomatal size in taxa that diversified under low CO2. Front. Plant Sci. 7, 1253.
[6] Kaiser, E., Kromdijk, J., Harbinson, J., et al., 2017. Photosynthetic induction and its diffusion, carboxylation and electron transport processes as affected by CO2 partial pressure, temperature, air humidity and blue irradiance. Ann. Bot. 119, 191-205.
[7] Kaiser, E., Morales, A., Harbinson, J., et al., 2016. Metabolic and diffusional limitations of photosynthesis in fluctuating irradiance in Arabidopsis thaliana. Sci. Rep. 6, 31252.
[8] Kato-Noguchi, H., 2020. Involvement of allelopathy in the invasive potential of Tithonia diversifolia. Plants-Basel. 9, 766.
[9] Knapp, A.K., Smith, W.K., 1987. Stomatal and photosynthetic responses during sun/shade transitions in subalpine plants:influence on water use efficiency. Oecologia. 74, 62-67.
[10] Laduke, J., 1982. Revision of Tithonia. Rhodora. 84, 453-522.
[11] Lawson, T., Blatt, M.R., 2014. Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency. Plant Physiol. 164, 1556-1570.
[12] Liu, W.J., Zhang, Y.P., Li, H.M., et al., 2004. Fog characteristics in a tropical seasonal rain forest in Xishuangbanna. Chin. J. Plant Ecol. 28, 264-270.
[13] Liu, J., Zhang, J., Estavillo, G.M., et al., 2021. Leaf N content regulates the speed of photosynthetic induction under fluctuating light among canola genotypes (Brassica napus L.). Physiol. Plantarum 172, 1844-1852.
[14] Morales, E., 2000. Estimating phylogenetic inertia in Tithonia (Asteraceae):a comparative approach. Evolution. 54, 475-484.
[15] Mott, K.A., Woodrow, I.E., 2000. Modelling the role of Rubisco activase in limiting non-steady-state photosynthesis. J. Exp. Bot. 51, 399-406.
[16] Obiakara, M.C., Fourcade, Y., 2018. Climatic niche and potential distribution of Tithonia diversifolia (Hemsl.) A. Gray in Africa. PLoS One. 13, e0202421.
[17] Otusanya, O.O., Ilori, O., 2012. Phytochemical screening and the phytotoxic effects of aqueous extracts of Tithonia diversifolia (hemsl) A. Gray. Int. J. Biol. 4, 97.
[18] Oyerinde, R.O., Otusanya, O.O., Akpor, O. B., 2009. Allelopathic effect of Tithonia diversifolia on the germination, growth and chlorophyll contents of maize (Zea mays L.). Sci. Res. Essays 4, 1553-1558.
[19] Pearcy, R.W., 1990. Sunflecks and photosynthesis in plant canopies. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41, 421-453.
[20] Pearcy, R.W. 1994. Photosynthetic Utilization of Sunflecks:A Temporally Patchy Resource on a Time Scale of Seconds to Minutes.
[21] R Core Team, 2020. R:A Language and Environment for Statistical Computing. R. Foundation for Statistical Computing, Vienna, Austria. Retrieved from. https://www.R-project.org/.
[22] Sakoda, K., Adachi, S., Yamori, W., et al., 2022. Towards improved dynamic photosynthesis in C3 crops by utilising natural genetic variation. J. Exp. Bot. 73, 3109-3121.
[23] Santelia, D., Lawson, T., 2016. Rethinking guard cell metabolism. Plant Physiol. 172, 1371-1392.
[24] Slattery, R.A., Walker, B.J., Weber, A.P.M., et al., 2018. The impacts of fluctuating light on crop performance. Plant Physiol. 176, 990-1003.
[25] Soleh, M.A., Tanaka, Y., Kim, S.Y., et al., 2017. Identification of large variation in the photosynthetic induction response among 37 soybean[Glycine max (L.) Merr.] genotypes that is not correlated with steady-state photosynthetic capacity. Photosynth. Res. 131, 305-315.
[26] Sudo, E., Makino, A. and Mae, T. 2003, Differences between rice and wheat in ribulose-1,5-bisphosphate regeneration capacity per unit of leaf-N content. Plant Cell Environ. 26, 255-263.
[27] Sun, H., Zhang, Y.Q., Zhang, S.B., et al., 2022. Photosynthetic induction under fluctuating light is affected by leaf nitrogen content in tomatoes. Front. Plant Sci. 13, 835571.
[28] Takashima, T., Hikosaka, K. and Hirose, T. 2004, Photosynthesis or persistence:nitrogen allocation in leaves of evergreen and deciduous Quercus species. Plant Cell Environ. 27:1047-1054.
[29] Tanaka, Y., Adachi, S., Yamori, W., 2019. Natural genetic variation of the photosynthetic induction response to fluctuating light environment. Curr. Opin. Plant Biol. 49, 52-59.
[30] Taylor, S.H., Long, S.P., 2017. Slow induction of photosynthesis on shade to sun transitions in wheat may cost at least 21% of productivity. Philos. Trans. R. Soc., B. 372, 20160543.
[31] Voelker, S.L., Brooks, J.R., Meinzer, F.C., et al., 2016. A dynamic leaf gas-exchange strategy is conserved in woody plants under changing ambient CO2:evidence from carbon isotope discrimination in paleo and CO2 enrichment studies. Global Change Biol. 22, 889-902.
[32] Xiong, Z., Xiong, D.L., Cai, D.T., et al., 2022. Effect of stomatal morphology on leaf photosynthetic induction under fluctuating light across diploid and tetraploid rice. Environ. Exp. Bot. 194, 104757.
[33] Zhang, Q., Peng, S.B., Li, Y., 2019. Increased rate of light-induced stomatal conductance is related to stomatal size in the Oryza genus. J. Exp. Bot. 70, 5259-5269.
[34] Zhu, X.G., Ort, D., Whitmarsh, J., et al., 2004. The slow reversibility of photosystem II thermal energy dissipation on transfer from high to low light may cause large losses in carbon gain by crop canopies:a theoretical analysis. J. Exp. Bot. 55, 1167-1175.