Growth but Not Photosynthesis Response of a Host Plant to Infection by a Holoparasitic Plant Depends on Nitrogen Supply

PLOS ONE, Dec 2019

Parasitic plants can adversely influence the growth of their hosts by removing resources and by affecting photosynthesis. Such negative effects depend on resource availability. However, at varied resource levels, to what extent the negative effects on growth are attributed to the effects on photosynthesis has not been well elucidated. Here, we examined the influence of nitrogen supply on the growth and photosynthesis responses of the host plant Mikania micrantha to infection by the holoparasite Cuscuta campestris by focusing on the interaction of nitrogen and infection. Mikania micrantha plants fertilized at 0.2, 1 and 5 mM nitrate were grown with and without C. campestris infection. We observed that the infection significantly reduced M. micrantha growth at each nitrate fertilization and more severely at low than at high nitrate. Such alleviation at high nitrate was largely attributed to a stronger influence of infection on root biomass at low than at high nitrate fertilization. However, although C. campestris altered allometry and inhibited host photosynthesis, the magnitude of the effects was independent of nitrate fertilizations. The infection reduced light saturation point, net photosynthesis at saturating irradiances, apparent quantum yield, CO2 saturated rate of photosynthesis, carboxylation efficiency, the maximum carboxylation rate of Rubisco, and maximum light-saturated rate of electron transport, and increased light compensation point in host leaves similarly across nitrate levels, corresponding to a similar magnitude of negative effects of the parasite on host leaf soluble protein and Rubisco concentrations, photosynthetic nitrogen use efficiency and stomatal conductance across nitrate concentrations. Thus, the more severe inhibition in host growth at low than at high nitrate supplies cannot be attributed to a greater parasite-induced reduction in host photosynthesis, but the result of a higher proportion of host resources transferred to the parasite at low than at high nitrate levels.

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Growth but Not Photosynthesis Response of a Host Plant to Infection by a Holoparasitic Plant Depends on Nitrogen Supply

Ye W-H (2013) Growth but Not Photosynthesis Response of a Host Plant to Infection by a Holoparasitic Plant Depends on Nitrogen Supply. PLoS ONE 8(10): e75555. doi:10.1371/journal.pone.0075555 Growth but Not Photosynthesis Response of a Host Plant to Infection by a Holoparasitic Plant Depends on Nitrogen Supply Hao Shen 0 Shu-Jun Xu 0 Lan Hong 0 Zhang-Ming Wang 0 Wan-Hui Ye 0 Gabriele Sorci, CNRS, Universite de Bourgogne, France 0 1 Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems , South China Botanical Garden , Chinese Academy of Sciences , Guangzhou, Guangdong , PR China , 2 College of Life Sciences, University of Chinese Academy of Sciences , Beijing , PR China , 3 College of Horticulture and Landscape Architecture, Zhongkai University of Agriculture and Engineering , Guangzhou, Guangdong , PR China Parasitic plants can adversely influence the growth of their hosts by removing resources and by affecting photosynthesis. Such negative effects depend on resource availability. However, at varied resource levels, to what extent the negative effects on growth are attributed to the effects on photosynthesis has not been well elucidated. Here, we examined the influence of nitrogen supply on the growth and photosynthesis responses of the host plant Mikania micrantha to infection by the holoparasite Cuscuta campestris by focusing on the interaction of nitrogen and infection. Mikania micrantha plants fertilized at 0.2, 1 and 5 mM nitrate were grown with and without C. campestris infection. We observed that the infection significantly reduced M. micrantha growth at each nitrate fertilization and more severely at low than at high nitrate. Such alleviation at high nitrate was largely attributed to a stronger influence of infection on root biomass at low than at high nitrate fertilization. However, although C. campestris altered allometry and inhibited host photosynthesis, the magnitude of the effects was independent of nitrate fertilizations. The infection reduced light saturation point, net photosynthesis at saturating irradiances, apparent quantum yield, CO2 saturated rate of photosynthesis, carboxylation efficiency, the maximum carboxylation rate of Rubisco, and maximum light-saturated rate of electron transport, and increased light compensation point in host leaves similarly across nitrate levels, corresponding to a similar magnitude of negative effects of the parasite on host leaf soluble protein and Rubisco concentrations, photosynthetic nitrogen use efficiency and stomatal conductance across nitrate concentrations. Thus, the more severe inhibition in host growth at low than at high nitrate supplies cannot be attributed to a greater parasite-induced reduction in host photosynthesis, but the result of a higher proportion of host resources transferred to the parasite at low than at high nitrate levels. - Funding: This work was funded by the National Key Technologies R&D Program of China (2012BAC07B04). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Parasitic plants are a taxonomically diverse group of organisms that obtain some or all of their nutrients and other resources, such as water, carbon and phytohormones, from their host plants via haustoria [1]. Interactions between them and their hosts are one of the key research topics in parasitic plant biology [2,3]. Press et al. [1] indicated that the extent to which parasites compete with their hosts for nutrients depends on the relative sink strength and the degree of autotrophy of the parasites. In hemiparasitic plants, nutrient transfer and resource acquisition from the hosts are facilitated by the parasite maintaining high transpiration rates, high leaf conductance and low water potentials, and in holoparasitic plants, by high osmotic potentials [3]. Furthermore, parasitic plants can affect the photosynthesis of their hosts at the leaf and/or whole plant level [4]. These processes can adversely affect the hosts, and such negative effects depend on resource availability: they might be negligible when resources are abundant but when resources are limiting they can be severe, ranging from reduction of growth and development to death of the hosts [3]. The influence of nitrogen on host-parasite associations has been investigated in the economically important root hemiparasite Striga hermonthica [5,6] and the stem holoparasite Cuscuta reflexa [7,8]. Striga hermonthica-infected C4 sorghum had lower rates of photosynthesis than uninfected plants, but the difference in both growth and photosynthesis between uninfected and infected sorghum plants was lower or even negligible when high nitrogen concentrations were supplied [5]. In contrast, high nitrogen supply did not result in an alleviation of the effects of the parasite on the host C3 rice to the same degree that S. hermo (...truncated)


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Hao Shen, Shu-Jun Xu, Lan Hong, Zhang-Ming Wang, Wan-Hui Ye. Growth but Not Photosynthesis Response of a Host Plant to Infection by a Holoparasitic Plant Depends on Nitrogen Supply, PLOS ONE, 2013, Volume 8, Issue 10, DOI: 10.1371/journal.pone.0075555