Progress and Problems in Producing Nitrogen Dioxide-Philic Plants

Document Type: Letter

Authors

Department of Mathematical and Life Sciences, Graduate School of Science, Hiroshima University, Higashi-Hiroshima, Japan

Abstract

The recently published articles in the Iranian Journal of Biotechnology inspired us to write this short communication on nitrogen dioxide NO2-philic plants (1). To cope with environmental pollution, we thought (still think) that development of methods that mitigate pollution is an urgent issue, and that NO2-philic plants that can grow with NO2 as the sole nitrogen source are instrumental for the implementation of mitigation of air pollution.

Keywords


The recently published articles in the Iranian Journal of
Biotechnology inspired us to write this short communication on nitrogen dioxide NO2-philic plants (1).
To cope with environmental pollution, we thought
(still think) that development of methods that mitigate
pollution is an urgent issue, and that NO2-philic plants
that can grow with NO2 as the sole nitrogen source are
instrumental for the implementation of mitigation of air
pollution.
The main point of this idea is that mitigation, rather
than monitoring or observation, of environmental pollution is of primary importance. In other words, our point
is that “plants that rely on pollution”, rather than “plants
that are resistant to pollution”, are more meaningful to
implement air remediation by plants. In the very beginning of this study, we attempted screening of such plants
among naturally occurring plants (2). Screening study revealed that several plant species have a high ability to uptake and assimilate NO2 (2). But it was not high enough
for these species to grow with NO2 as the sole nitrogen
source (3). We also performed genetic engineering of nitrite reductase (NiR), which is a second enzyme of nitrate
reduction pathway and a key enzyme of assimilation
of NO2. We have produced genetically modifid plants
of Arabidopsis thaliana (a model plant species) (4) and
Rhaphiolepis umbellata (a roadside tree species) (5) that
signifiantly bear higher NiR activities compared with
non-transformed control plants. However, their ability
to uptake NO2 was less than two times higher than that
of non-tranformed plants, and again this was not enough
for them to be NO2-philic (3).
We also investigated the growth of plants in the presence of NO2 as the sole nitrogen source, using Nicotiana
plumbaginifolia as a test species. The Plants were grown in
the complete absence of root nitrogen under exposure to
0, 0.15, 1.0 and 4.0 ppm NO2 and natural light at 22°C for 9
– 13 weeks. Control plants were grown with 10 mM KNO3 in
ambient air containing < 0.05 ppm NO2. Plants grown at
0 ppm NO2 died after 6 weeks. The relative growth rate in
biomass (RGR) of plants grown at 1.0 Pm NO2 and that of
those grown at 4.0 ppm NO2 were very similar to the RGR
of control plants (about 0.1.day -1). However, plants grown
at 1.0 and 4.0 ppm NO2 exhibited some morphological abnormalities in leaves (Figure 1, Nakagawa, Takahashi and
Morikawa, unpublished results), that indicates the toxic
effcts of NO2. Interestingly, plants grow n at 0.15 ppm
NO2 did not show such damages and grew normally up
to 13 weeks. Furthermore, we also noticed that NO2 at 0.15
ppm is somewhat stimulatory for the growth of plants.


Clearly, the effct of NO2 on plant growth changes as a
function of its concentrations; it was inhibitory at high
concentrations but stimulatory at low concentrations.
Thus, clarifiation of these toxic and stimulatory effcts of

NO2 may provide an important key to produce NO2-philic
plants. The investigation on the stimulatory effct of NO2
led to the fiding of a plant-hormone like effct of NO2 on
the growth and development of plants (6). Ambient concentrations of NO2 stimulated growth and biomass production of plants that were well fed root nitrogen. Uptake
per plant of nutrients was also stimulated. Carbon and nitrogen metabolisms also were stimulated by the presence
of NO2. This effct was confimed in several plant species
including Arabidopsis and horticultural species (3).
The investigation on the toxic effct of NO2 led us to the
investigation on metabolic fate of NO2 in plants, and to
the fiding of novel oxidized nitrogen compounds including nitro- and nitroso-organic compounds formed
from NO2 (7, 8). We also found that fumigation of Arabidodpsis plants with a high concentration (4 - 40 ppm)
of NO2 induces nitration of specifi proteins involved in
photosystem II in chloroplasts (Takahashi and Morikawa,
submitted). Protein tyrosine nitration is an important
posttranslational protein modifiation, and thus protein
nitration induced by NO2 may be of important biological relevance. Currently, which one(s) of such nitro- and
nitroso-organic compounds including nitrated proteins
is responsible to the toxic effct of NO2 has yet to be identifid. Nonetheless, the abovementioned results on these
two effcts of NO2 implicate that exogenous NO2 plays
a distinct role in cellular signaling. Clarifiation of the
mechanisms and identifiation of genes involved in both
toxic and stimulatory effcts of NO2 will pave the way for
production of NO2-philic plants for air remediation.
Acknowledgements
We thank Professor Christian Meyer, Unite´ de Nutrition Azote´e des Plantes, Institut Jean-Pierre Bourgin,
INRA Versailles, Versailles, France for his interest in our
study and providing seeds of Nicotiana plumbaginifolia.
Authors’ Contribution
Misa Takahashi developed the original idea and the
protocol, abstracted and analyzed data, wrote the manuscript, and are guarantor. Hiromichi Morikawa developed the idea, abstracted, and wrote the manuscript together with M.T. Makiko Nakagawa mainly contributed
to the analysis of data.
Financial Disclosure
No relevant fiancial interests or fiancial conflcts
within the past 5 years and for the foreseeable future.



1. Morikawa H, Takahashi M, Hakata M, Sakamoto A. Screening and
genetic manipulation of plants for decontamination of pollutants from the environments. Biotechnol Adv. 2003;22(1-2):9-15.
2. Morikawa H, Higaki A, Nohno M, Takahashi M, Kamada M, Nakata
M, et al. More than a 600-fold variation in nitrogen dioxide assimilation among 217 plant taxa. Plant Cell Envir. 1998;21(2):180-
90.
3. Takahashi M, Morikawa H. J Envir Protect Air-Pollut Philic Plants
Air Remediation. 3 2012:1346-52.
4. Takahashi M, Sasaki Y, Ida S, Morikawa H. Nitrite reductase gene
enrichment improves assimilation of NO(2) in Arabidopsis. Plant
Physiol. 2001;126(2):731-41.
5. Shigeto J, Yoshihara S, Adam SEH, Sueyoshi K, Sakamoto A,
Morikawa H, et al. Genetic engineering of nitrite reductase
gene improves uptake and assimilation of nitrogen dioxide
by Rhaphiolepis umbellata (Thunb.) Makino. Plant Biotech.
2006;23(1):111-6.
6. Takahashi M, Nakagawa M, Sakamoto A, Ohsumi C, Matsubara
T, Morikawa H. Atmospheric nitrogen dioxide gas is a plant vitalization signal to increase plant size and the contents of cell
constituents. New Phytol. 2005;168(1):149-54.
7. Morikawa H, Takahashi M, Sakamoto A, Matsubara T, Arimura
G, Kawamura Y, et al. Formation of unidentifid nitrogen in
plants: an implication for a novel nitrogen metabolism. Planta.
2004;219(1):14-22.
8. Morikawa H, Takahashi M, Sakamoto A, Ueda-Hashimoto M,
Matsubara T, Miyawaki K, et al. Novel metabolism of nitrogen in
plants. Z Naturforsch C. 2005;60(3-4):265-71.