Plants adapt to environmental changes: How and Why?
Research by Kouki Hikosaka
(14 June 2016)
Japanese version is here.
Lessons from natural variation: intraspecific variation as a model system to study local adaptation
There are quantitative variation in many plant traits even within a species. Some of them are a result of adaptation to their habitat: optimal strategy (or evolutionarily stable strategy) may differ depending on environmental conditions, leading to trait differentiations between ecotypes. We have studied both genetic and phenotypic variation along gradients of latitude (Ishikawa et al. 2007), altitude (Kubota et al. 2015), atmospheric CO2 concentration using natural CO2 springs (see below) and worldwide (Oguchi et al. 2016). We study traits and genes that are associated with adaptation to specific environmental factors. We also try to create a plant that is adapted to desired environment.
A leaf of a lowland ecotype (left) and a highland ecotype of Arabidopsis halleri
Ecology and evolution around natural CO2 spring
Atmospheric CO2 concentration is increasing and is predicted to reach 700 ppm at the end of this century. So far many studies have been conducted on plant responses to elevated CO2 concentration but most of them implicitly assume that future plants respond to elevated CO2 as current plants do. We hypothesize that elevated CO2 act as a selective agent and future plants may have different traits from those of current ones. We study plants growing around natural CO2 springs where they have been exposed to high CO2 concentrations for long term. We have described in-situ plant traits at high and normal CO2 concentrations around CO2 springs (Onoda et al. 2007, Osada et al. 2010). We also conducted common-garden experiments and showed that there are phenotypic and genetic differences between plants inhabiting high and normal CO2 concentrations (Onoda et al. 2009, Nakamura et al. 2011), suggesting that local evolution has occurred in high CO2 area around CO2 springs.
Interspecific difference in the photosynthesis-nitrogen relationship
It is well known that, within a species, photosynthetic capacity of leaves is strongly correlated to the leaf nitrogen content. However, the slope of the regression differs among species. When the leaves with same nitrogen contents are compared, the photosynthetic capacity of herbs (open symbols) is twice higher than that of evergreen trees (closed symbols). Hikosaka et al. (1998a) investigated the causes of difference in photosynthetic nitrogen use efficiency PNUE, (photosynthetic capacity per unit nitrogen) between Chenopodium album (an annual) and Quercus myrsinaefolia (an evergreen tree). Chenopodium album had the photosynthetic capacity twice higher than Q. myrsinaefolia. This difference was due to differences in 1) the drop of CO2 concentration between air and the intercellular space, 2) the drop of CO2 concentration between the intercellular space and the chloroplasts, 3) allocation of nitrogen into a key enzyme of photosynthesis (Rubisco), and 4) the specific activity of Rubisco. However, quantitative difference of each factor was small. We concluded that the difference in several factors causes large difference in photosynthetic nitrogen use efficiency.
What is the advantage in species with low PNUE? Takashima et al. (2004) studied nitrogen partitioning in deciduous and evergreen Quercus species. Evergreen leaves were found to allocate more leaf nitrogen to detergent-insoluble proteins (assumed as cell-wall proteins). Onoda et al. (2004) also found that early germinator of Poligonum cuspidatam allocates more leaf nitrogen to cell walls than late germinator. Nitrogen partitioning to cell-wall proteins was positively correlated with leaf mass per area in both studies, suggesting a trade-off between protection and photosynthesis.
We studied the contents of Rubisco (a key enzyme of photosynthesis) and cell walls in leaves of 26 species with a large variation in photosynthetic rates (Hikosaka and Shigeno 2009). We focused on photosynthetic nitrogen-use effciency (PNUE, photosynthetic rate per nitrogen), which can be expressed as the product of Rubisco-use effciency (RBUE, photosynthetic rate per Rubisco) and Rubisco nitrogen fraction (RNF, Rubisco nitrogen per total leaf nitrogen). RBUE accounted for 70% of the interspecific variation in PNUE. The variation in RBUE was ascribed partly to stomatal conductance, and other factors such as mesophyll conductance and Rubisco kinetics might also be involved. RNF was also significantly related to PNUE but the correlation was relatively weak. Cell wall nitrogen fraction (WNF, cell wall nitrogen per total leaf nitrogen) increased with increasing leaf mass per area, but there was no correlation between RNF and WNF. These results suggest that nitrogen allocation to cell walls does not explain the variation in PNUE. The difference in PNUE was not caused by a sole factor that was markedly different among.
See Hikosaka (2004, 2010) for review of interspecific difference in PNUE.
Temperature acclimation of the photosynthetic apparatus
It is well known that temperature dependence of the photosynthetic rate changes depending on growth temperatures. Hikosaka (1997) proposed a hypothesis that the change in organization of the photosynthetic apparatus possibly contribute to the change in the temperature dependence of photosynthesis. Hikosaka et al. (1999b) investigated gas exchange characteristics of Qercus myrsinaefolia, an evergreen tree, grown under contrasting temperatures. It was revealed that the change in temperature dependence of photosynthesis involves changes in temperature dependence of two processes, carboxylation and regeneration of RuBP, and change in the balance between the two processes. Hikoska (2005b) found that Plantago asiatica leaves invested more nitrogen in regeneration process when they were grown at low temperature. These results are consistent with the prediction of Hikosaka (1997).
See a review article: Hikosaka et al. (2006).
Nitrogen partitioning among photosynthetic components
The photosynthetic system consists of many components. Their organization varies depending on growth conditions. In particular, it is well known that the organization changes with growth irradiance. Hikosaka and Terashima (1995) proposed a mathematical model to calculate optimal organization of photosynthetic components under different light conditions. In this model, leaf nitrogen is regarded as a resource and optimal nitrogen partitioning among photosynthetic components to maximize daily photosynthesis is considered. It was predicted that the fraction of chlorophyll-protein complexes increases and the fraction of Calvin cycle enzymes and electron carriers decreases with decreased light availability. This prediction was consistent with actual responses in organization of photosynthetic components.
Hikosaka and Terashima (1996) investigated organization of photosynthetic components in a sun species Chenopodium album and a shade species Alocasia odora grown at 5, 10, 30, 50, and 100% of full sunlight and compared it with the theoretical prediction. Except for C. album grown under 5% condition, actual organization was quite similar to the predicted one. It was concluded that both species can regulate their photosynthetic apparatus under wide range of light environment.
I studied for theoretical relationship between optimal organization of photosynthetic apparatus and changes in growth condition other than light. Hikosaka (1997) showed that changes in organization of photosynthetic apparatus is possibly effective to increase carbon gain under different temperature conditions and that changes in the temperature-response curve of photosynthesis can be explained by changes in organization of photosynthetic components. Hikosaka and Hirose (1998) predicted effects of organization of photosynthetic components on carbon gain of leaf and canopy under the high CO2 condition. At 25C, leaf photosynthesis will increase 40% by doubling of CO2 concentration without any changes in the photosynthetic apparatus. If nitrogen partitioning among photosynthetic components change optimally, the increase in leaf photosynthesis by doubling CO2 level will become 60%. The increase of leaf photosynthesis by doubling CO2 level will be enhanced at higher temperature.
Resource acquisition and use in plant communities
There have been many studies for intraspecific competition. However, although it has been recognized that resource acquisition and utilization are important for competition, there were few studies to evaluate how much individuals acquire resources and how efficient the acquired resources are used. One of main theme in our laboratory is to clarify the mechanisms of competition in plant canopies using a canopy photosynthesis model. Hikosaka and Hirose (1997) predicted that horizontal leaves are evolutionarily stable under light competition and vertical leaves are advantageous in canopies of clonal plants in which light competition is not severe. The solution of the evolutionarily stable stratedy is expected to vary depending on degree of 'interaction' between individuals. Hikosaka et al. (2001) proposed a simple formulation to determine the 'interaction' in competition for light and a method to evaluate the interaction in actual stands.
Using a canopy photosynthesis model, we determined photosynthesis of individuals in a natural monospecific stand of Xanthium canadense (Hikosaka et al. 1999a, Matsumoto et al. 2008). The estimated photosynthesis was well correlated with plant growth rate. The relative photosynthetic rate (photosynthesis per unit aboveground mass) was higher in larger individuals. This suggests that competition in the stand was asymmetric (one-sided). However, among larger individuals, the relative photosynthetic rate was similar to each other, suggesting the competitive symmetry (two-sided). We also investigated nitrogen dynamics in plants of the same stand (Hikosaka and Hirose 2001). Both nitrogen productivity (growth rate per nitrogen in plant) and mean residence time of nitrogen within the plant were higher in larger individuals. This suggests that nitrogen use efficiency (growth per absorbed nitrogen) is higher in larger individuals. Nitrogen uptake rates were higher in larger individuals and its relation with plant size was curvilinear, suggesting that competition for nitrogen in soil between individuals was asymmetric. However, the competition for nitrogen was more symmetric compared with that for light. Resource acquisition and use in competing plants under elevated CO2 conditions were also assessed (Nagashima et al. 2003, Hikosaka et al. 2003).
Effects of light and leaf age on photosynthetic characteristics
It is known that photosynthetic characteristics vary with light environment or with leaf age. In erect herbaceous plants, old leaves tend to be shaded by younger leaves expanding. In previous studies for leaf senescence, effects of light and age were not investigated separately. I raised a vine (Ipomoea tricolor Cav.) horizontally to avoid mutual shading by leaves. Hikosaka et al. (1992, 1993, 1994) investigated the effect of light and age on leaf nitrogen content. Without any shading, leaf nitrogen content was stable in plants grown under high nutrient availability but decreased with age in plants grown under low nutrient availability. When plants were grown under which older leaves receive weaker light intensity (canopy-type shading), leaf nitrogen content was lower in older shaded leaves. When plants were grown under which older leaves receive stronger light intensity (inversed canopy-type shading), leaf nitrogen was higher in older leaves. It was concluded that both leaf age and light are responsible for leaf nitrogen content and that leaf nitrogen content is very flexible with changes in light conditions.
Hikosaka (1996) investigated effects of light and leaf age on organization of photosynthetic components. Organization of photosynthetic components is important for optimal carbon gain of leaves (see below). There have been many reports that organization of photosynthetic components is affected by light and by leaf age. Using I. tricolor plants, I revealed that organization of photosynthetic components is affected by light, not by leaf age.
Light is indispensable for photosynthesis but excessively strong light can cause damage in the photosynthetic apparatus (photoinhibition). We studied determinants of the rate of photoinhibition in leaves. First we established an experimental system where detached leaves are subjected to photoinhibitory treatment with nearly-natural conditions. We showed that leaf discs floated on water are different to intact leaves in photosynthesis and photoinhibition (Kato et al. 2002a). Second we investigated contribution of recovery of damaged PSII to photoprotection in leaves grown different light and nutrient availabilities. Leaves grown at high light were more tolerant to photoinhibition with and without the recovery of damaged PSII irrespective of nutrient conditions. The rate constant of the recovery was higher in high-light grown leaves (Kato et al. 2002b). We further studied chl fluorescence parameters in the leaves. We used a model of light partitioning in leaves. We found that the excess energy that is neither utilized in photosynthesis nor dissipated as heat was strongly correlated with the rate constant of photoinactivation (damage without recovery), suggesting the excess energy determines the photoinactivation rate (Kato et al. 2003). We determined temperature dependence of the rate constant of recovery and photoinactivation, electron transport, heat dissipation, and excess energy (Tsonev and Hikosaka 2003). Photosynthetic rates and photon partitioning in photoinhibited leaves were studied (Hikosaka et al. 2004).
PDF files for papers published are avaiable. Mail to hikosakaATm.tohoku.ac.jp
1) Hikosaka K, Terashima I, Katoh S (1994) Effects of leaf age, nitrogen nutrition and photon flux density on the distribution of nitrogen among leaves of a vine (Ipomoea tricolor Cav.) grown horizontally to avoid mutual shading of leaves. Oecologia, 97: 451-457. [Springer]
2) Hikosaka K, Terashima I (1995) A model of the acclimation of photosynthesis in the leaves of C3 plants to sun and shade with respect to nitrogen use. Plant, Cell & Environment, 18: 605-618. [Blackwell]
3) Terashima I, Hikosaka K (1995) Comparative ecophysiology of leaf and canopy photosynthesis. Plant, Cell & Environment, 18: 1111-1128. [Blackwell]
4) Hikosaka K (1996) Effects of leaf age, nitrogen nutrition and photon flux density on the organization of the photosynthetic apparatus in leaves of a vine (Ipomoea tricolor Cav.) grown horizontally to avoid mutual shading of leaves. Planta, 198: 144-150. [Springer]
5) Hikosaka K, Terashima I (1996) Nitrogen partitioning among photosynthetic components and its consequence in sun and shade plants. Functional Ecology, 10: 335-343.
6) Funayama S, Hikosaka K, Yahara T (1997) Effects of virus infection and growth irradiance on fitness components and photosynthetic properties of Eupatorium makinoi (Compositae). American Journal of Botany, 84: 823-829. [AmJBot]
7) Hikosaka K, Hirose T (1997) Leaf angle as a strategy for light competition: Optimal and evolutionarily stable light-extinction coefficients within a canopy. Écoscience, 4: 501-507. [Ecoscience]
8) Hikosaka K (1997) Modelling optimal temperature acclimation of the photosynthetic apparatus in C3 plants with respect to nitrogen use. Annals of Botany, 80: 721-730. [Oxford] [PDF]
9) Anten NPR, Miyazawa K, Hikosaka K, Nagashima H, Hirose T (1998) Leaf nitrogen distribution in relation to leaf age and photon flux density in dominant and subordinate plants in dense stands of a dicotyledonous herb. Oecologia, 113: 314-324. [Springer]
10) Hikosaka K, Hirose T (1998) Leaf and canopy photosynthesis of C3 plants at elevated CO2 in relation to optimal partitioning of nitrogen among photosynthetic components: theoretical prediction. Ecological Modelling, 106: 247-259. [ScienceDirect]
11) Hikosaka K, Hanba YT, Hirose T, Terashima I (1998a) Photosynthetic nitrogen-use efficiency in woody and herbaceous plants. Functional Ecology, 12: 896-905. [Blackwell] [PDF]
12) Hikosaka K, Sudoh S, Hirose T (1999a) Light acquisition and use of individuals competing in a dense stand of an annual herb, Xanthium canadense. Oecologia, 118: 388-396. [Springer]
13) Hikosaka K, Murakami A, Hirose T (1999b) Balancing carboxylation and regenaration of ribulose-1,5-bisphosphate in leaf photosynthesis in temperature acclimation of an evergreen tree, Quercus myrsinaefolia. Plant, Cell & Environment, 22: 841-849. [Blackwell] [PDF]
14) Hikosaka K, Hirose T (2000a) Photosynthetic nitrogen use efficiency in species coexisting in a warm-temperate evergreen forest. Tree Physiology, 20: 1249-1254. [Heron]
15) Hikosaka K, Hirose T (2001) Nitrogen uptake and use by competing individuals in a Xanthium canadense stand. Oecologia 126: 174-181. [Springer]
16) Hikosaka K, Nagashima H, Harada Y, Hirose T (2001) A simple formulation of interaction between individuals competing for light in a monospecific stand. Functional Ecology, 15: 642-646. [Blackwell] [PDF]
17) Hikosaka K, Nagamatsu D, Ishii HS, Hirose T (2002) Photosynthesis-nitrogen relationships in species at different altitudes of Mount Kinabalu, Malaysia. Ecological Research, 17: 305-313. [Springer]
18) Kato MC, Hikosaka K, Hirose T (2002a) Leaf discs floated on water are different from intact leaves in photosynthesis and photoinhibition. Photosynthesis Research, 72: 65-70. [Springer]
19) Kato MC, Hikosaka K, Hirose T (2002b) Photoinactivation and recovery of photosystem II of Chenopodium album leaves grown at different levels of irradiance and nitrogen availability. Functional Plant Biology (formerly Australian Journal of Plant Physiology), 29: 787-795. [CSIRO]
20) Werger MJA, Hirose T, During HJ, Heil GW, Hikosaka K. Ito T, Nachinshonhor, Shibazaki K, Nagamatsu D, Takatsuki S, Anten NPR (2002) Light partitioning among species and species replacement in early successional grasslands. Journal of Vegetation Science, 13: 615-626. [PDF]
21) Yasumura Y, Hikosaka K, Matsui K, Hirose T (2002) Leaf-level nitrogen-use efficiency of canopy and understorey species in a beech forest. Functional Ecology , 16: 826-834. [Blackwell] [PDF]
22) Kato MC, Hikosaka K, Hirotsu N, Makino A, Hirose T (2003) The excess light energy that is neither utilized in photosynthesis nor dissipated by photoprotective mechanisms determines the rate of photoinactivation in photosystem II. Plant and Cell Physiology, 44: 318-325. [Oxford]
23) Oguchi R, Hikosaka K, Hirose T (2003) Does the photosynthetic light-acclimation need change in leaf anatomy? Plant, Cell and Environment, 26: 505-512. [Blackwell] [PDF]
24) Nagashima H, Yamano T, Hikosaka K, Hirose T (2003) Effects of elevated CO2 on the size structure in even-aged monospecific stands of Chenopodium album. Global Change Biology. 9: 619-629. [Blackwell]
25) Ishizaki S, Hikosaka K, Hirose T (2003) Increase in leaf mass per area benefits plant growth at elevated CO2 concentration. Annals of Botany, 91: 905-914. [Oxford] [PDF]
26) Hikosaka K (2003) A model of dynamics of leaves and nitrogen in a plant canopy: an integration of canopy photosynthesis, leaf life span, and nitrogen use efficiency. American Naturalist, 162: 149-164. [UnivChicagoPress]
27) Tsonev TD, Hikosaka K (2003) Contribution of photosynthetic electron transport, heat dissipation, and recovery of photoinactivated photosystem II to photoprotection at different temperatures in Chenopodium album leaves. Plant and Cell Physiology, 44: 828-835. [Oxford]
28) Kinugasa T, Hikosaka K, Hirose T (2003) Reproductive allocation of an annual, Xanthium canadense, at an elevated carbon dioxide concentration. Oecologia,137: 1-9. [Springer]
29) Hikosaka K, Yamano T, Nagashima H, Hirose T (2003) Light acquisition and use of individuals as influenced by elevated CO2 in even-aged monospecific stands of Chenopodium album. Functional Ecology, 17: 786-795. [Blackwell] [PDF]
30) Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavendar-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee B, Lusk C, Midgley JJ, Navas M-L, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature, 428: 821-827. [PDF]
31) Onoda Y, Hikosaka K, Hirose T (2004) Allocation of nitrogen to cell walls decreases photosynthetic nitrogen-use efficiency. Functional Ecology, 18:419-425. [Blackwell] [PDF]
32) Oikawa S, Hikosaka K, Hirose T, Hori Y, Shiyomi M, Takahashi S (2004) Cost-benefit relationships in leaves emerging at different times in a deciduous fern Pteridium aquilinum. Canadian Journal of Botany, 82: 521-527. [NRC]
33) Takashima T, Hikosaka K, Hirose T (2004) Photosynthesis or persistence: nitrogen allocation in leaves of evergreen and deciduous Quercus species. Plant, Cell and Environment, 27: 1047-1054. [Blackwell] [PDF]
34) Hikosaka K, Kato MC, Hirose T (2004) Photosynthetic rates and partitioning of absorbed light energy in photoinhibited leaves. Physiologia Plantarum, 121: 699-708. [Blackwell]
35) Hikosaka K (2004) Interspecific difference in the photosynthesis-nitrogen relationship: patterns, physiological causes, and ecological importance. Journal of Plant Research, 117: 481-494. [Springer]
36) Hikosaka K (2005) Leaf canopy as a dynamic system: ecophysiology and optimality in leaf turnover. Annals of Botany, 95: 521-533. [Oxford] [PDF]
37) Onoda Y, Hikosaka K, Hirose T (2005a) Seasonal change in the balance between capacities of RuBP carboxylation and RuBP regeneration affects CO2 response of photosynthesis in Polygonum cuspidatum. Journal of Experimental Botany, 56: 755-763. [Oxford] [PDF]
38) Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Garnier E, Hikosaka K, Lamont BB, Lee W, Oleksyn J, Osada N, Poorter H, Villar R, Warton DI, Westoby M (2005a) Assessing the generality of global leaf trait relationships. New Phytologist, 166: 485-496. [Blackwell] [PDF]
39) Hikosaka K, Takashima T, Kabeya D, Hirose T, Kamata N (2005a) Biomass allocation and leaf chemical defense in defoliated seedlings of Quercus serrata with respect to carbon-nitrogen balance. Annals of Botany, 95: 1025-1032. [Oxford] [PDF]
40) Hikosaka K, Onoda Y, Kinugasa K, Anten NPR, Nagashima H, Hirose T (2005b) Plant responses to elevated CO2 concentration at different scales: leaf, whole plant, canopy, and population. Ecological Research, 20: 243-253. [Springer]
41) Yasumura Y, Onoda Y, Hikosaka K, Hirose T (2005) Nitrogen resorption from leaves under different growth irradiance in three deciduous woody species. Plant Ecology, 178: 29-37. [Springer]
42) Kinugasa T, Hikosaka K, Hirose T (2005) Respiration and reproductive effort in Xanthium canadense. Annals of Botany, 96: 81-89. [Oxford] [PDF]
43) Oguchi R, Hikosaka K, Hirose T (2005) Leaf anatomy as a contraint for photosynthetic acclimation: differential responses in leaf anatomy to increasing growth irradiance among three deciduous trees. Plant, Cell and Environment, 28: 916-927. [Blackwell] [PDF]
44) Muller O, Hikosaka K, Hirose T (2005) Seasonal changes in light and temperature affect the balance between light utilisation and light harvesting components of photosynthesis in an evergreen understorey. Oecologia, 143: 501-508. [Springer]
45) Oikawa S, Hikosaka K, Hirose T (2005) Dynamics of leaf area in a canopy of an annual herb, Xanthium canadense. Oecologia, 143: 517-526. [Springer]
46) Hikosaka K (2005b) Nitrogen partitioning in the photosynthetic apparatus of Plantago asiatica leaves grown at different temperature and light conditions: similarities and differences between temperature and light acclimation. Plant and Cell Physiology, 46: 1283-1290. [Oxford]
47) Wright IJ, Cornelissen JHC, Falster DS, Groom PK, Hikosaka K, Lee W, Lusk CH, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Reich PB, Warton DI, Westoby M (2005b) Modulation of leaf economic traits and trait relationships by climate. Global Ecology and Biogeography, 14: 411-421. [Blackwell]
48) Onoda Y, Hikosaka K, Hirose T (2005b) The balance between RuBP carboxylation and RuBP regeneration: a mechanism underlying the interspecific variation in acclimation of photosynthesis to seasonal change in temperature. Functional Plant Biology, 32: 903-910. [CSIRO]
49) Onoda Y, Hikosaka K, Hirose T (2005) Natural CO2 springs in Japan: a case study of vegetation dynamics. Phyton 45: 389-394.
50) Kinugasa T, Hikosaka K, Hirose T (2005 ) Reproduction and respiration in an annual under elevated CO2. Phyton 45: 415-418.
51) Hikosaka K, Ishikawa K, Borjigidai A, Muller O, Onoda Y (2006) Temperature acclimation of photosynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rate. Journal of Experimental Botany, 57: 291-302. [Oxford] [PDF]
52) Borjigidai A, Hikosaka K, Hirose T, Hasegawa T, Okada M, Kobayashi K (2006) Sesonal changes in temperature dependence of photosynthetic rate in rice under a free-air CO2 enrichment. Annals of Botany, 97: 549-557. [Oxford] [PDF]
53) Yasumura Y, Hikosaka K, Hirose T (2006a) Resource allocation to vegetative and reproductive growth in relation to mast seeding in Fagus crenata. Forest Ecology and Management, 229: 228-233. [ScienceDirect]
54) Yasumura Y, Hikosaka K, Hirose T (2006b) Seasonal changes in photosynthesis, nitrogen content and nitrogen partitioning in Lindera umbellata leaves grown under high or low irradiance. Tree Physiology, 26: 1315-1323. [Heron]
55) Oikawa S, Hikosaka K, Hirose T (2006) Leaf life span and lifetime carbon gain of individual leaves in a stand of an annual herb, Xanthium canadense. New Phytologist, 172: 104-116. [Blackwell] [PDF]
56) Oguchi R, Hikosaka K, Hiura T, Hirose T (2006) Leaf anatomy and light acclimation in woody seedlings after gap formation in a cool-temperate deciduous forest. Oecologia, 149: 571-582. [Springer]
57) Hikosaka K, Nabeshima E, Hiura T (2007) Seasonal changes in temperature response of photosynthesis in canopy leaves of Quercus crispula in a cool-temperate forest. Tree Physiology, 27: 1035-1041. [Heron]
58) Onoda Y, Hirose T, Hikosaka K (2007) Effect of elevated CO2 on leaf starch, nitrogen and photosynthesis of plants growing at three natural CO2 springs in Japan. Ecological Research, 22: 574-484. [Springer] [PDF]
59) Yasumura Y, Hikosaka K, Hirose T (2007) Nitrogen resorption and protein degradation during leaf senescence in Chenopodium album grown in different light and nitrogen conditions. Functional Plant Biology, 34: 409-417. [CSIRO]
60) Miyagi KM, Kinugasa T, Hikosaka K, Hirose T (2007) Elevated CO2 concentration, nitrogen use, and seed production in annual plants. Global Change Biology, 13: 2161-2170. [Blackwell]
61) Ishikawa K, Onoda Y, Hikosaka K (2007) Intraspecific variation in temperature dependence of gas exchange characteristics of Plantago asiatica ecotypes from different temperature regimes. New Phytologist, New Phytologist, 176: 356-364. [Wiley]
62) Motomura H, Hikosaka K, Suzuki M (2008) Relationships between photosynthetic activity and silica accumulation with age of leaf in Sasa veitchii (Poaceae, Bambusioideae). Annals of Botany, 101: 463-468. [Oxford]
63) Oguchi R, Hikosaka K, Hiura T, Hirose T (2008) Costs and benefits of photosynthetic light acclimation of tree seedlings in response to gap formation. Oecologia, 155: 665-675. [Springer]
64) Oikawa S, Hikosaka K, Hirose T (2008) Does leaf shedding increase the whole-plant carbon gain despite some nitrogen being lost with shedding? New Phytologist, 178: 617-624. [Blackwell]
65) Matsumoto Y, Oikawa S, Yasumura Y, Hirose T, Hikosaka K (2008) Reproductive yield of individuals competing for light in a dense stand of Xanthium canadense. Oecologia, 157: 185-195. [Springer]
66) Yamori W, Noguchi K, Hikosaka K, Terashima I (2009) Cold tolerant crop species have greater temperature homeostasis of leaf respiration and photosynthesis than cold sensitive species. Plant and Cell Physiology, 50: 203-215. [Oxford]
67) Onoda Y, Hirose T, Hikosaka K (2009) Does photosynthesis adapt to CO2-enriched environments? An experiment on plants originating from three natural CO2 springs. New Phytologist, 182: 698-709. [Wiley].
68) Hikosaka K, Osone Y (2009) A paradox of leaf-trait convergence: why is leaf nitrogen concentration higher in species with higher photosynthetic capacity? Journal of Plant Research, 122: 245-251. [Springer].
68) Hikosaka K, Shigeno A (2009) The role of Rubisco and cell walls for the interspecific variation in photosynthetic capacity. Oecologia, 160:443-451. [Springer]
69) Borjigidai A, Hikosaka K, Hirose T (2009) Carbon balance in a monospecific stand of an annual herb Chenopodium album at an elevated CO2 concentration. Plant Ecology, 203: 33-44. [Springer]
70) Muller O, Oguchi R, Hirose T, Werger MJA, Hikosaka K (2009) The leaf anatomy of a broad-leaved evergreen allows an increase in nitrogen content in winter. Physiologia Plantarum, 136:299-309. [Wiley]
71) Nagano S, Nakano T, Hikosaka K, Maruta E (2009) Needle traits of evergreen coniferous shrub growing at wind-exposed and protected sites in a mountain region: Does Pinus pumila produce needles with greater mass per area under wind-stress conditions. Plant Biology, 11:94-100. [Wiley]
72) Yamori W, Noguchi K, Hikosaka K, Terashima I (2010) Phenotypic plasticity in photosynthetic temperature acclimation among crop species with different cold tolerances. Plant Physiology,15: 388-399 [Plant Physiology].
73) Oikawa S, Miyagi K-M, Hikosaka K, Okada M, Matsunami T, Kokubun M, Kinugasa T, Hirose T (2010) Interactions between elevated CO2 and N2-fixation determine soybean yield - a test using non-nodulated murant. Plant and Soil, 330: 163-172. [Springer]
74) Hikosaka K (2010) Mechanisims underlying interspecific variation in photosynthetic capacity across wild plant species. Plant Biotechnology, 27: 223-229. [J-Stage] [PDF]
75) Osada N, Onoda Y, Hikosaka K (2010) Effects of atmospheric CO2 concentration, irradiance and soil nitrogen availability on leaf photosynthetic traits on Polygonum sachalinense around the natural CO2 springs in northern Japan. Oecologia, 164-41-52. [Springer]
76) Kamiyama C, Oikawa S, Kubo T, Hikosaka K (2010) Light interception in species with different functional groups coexisting in moorland plant communities. Oecologia, 164: 591-599. [Springer]
78) Hikosaka K, Kawauchi Y, Kurosawa T (2010) Why does Viola hondoensis (Violaceae) shed its winter leaves in spring? American Journal of Botany, 97: 1944-1950. [AmerJBot]
79) Hikosaka K, Kinugasa T, Oikawa S, Onoda Y, Hirose T (2011) Effects of elevated CO2 concentration on seed production in C3 annual plants. Journal of Experimental Botany, 62: 1523-1530. [Oxford]
80) Nakamura I, Onoda Y, Matsushima N, Yokoyama J, Kawata M, Hikosaka K (2011) Phenotypic and genetic differences in a perennial herb across a natural gradient of CO2 concentration. Oecologia, 165: 809-818. [Springer]
81) Nagashima H, Hikosaka K (2011) Plants in a crowded stand regulate their height growth so as to maintain similar heights to neighbours even when they have potential advantages in height growth. Annals of Botany, 108: 207-214. [Oxford]
82) Muller O, Hirose T, Werger MJA, Hikosaka K (2011) Optimal use of leaf nitrogen explains seasonal change in leaf nitrogen content of an understory evergreen shrub. Annals of Botany, 108: 529-536. [Oxford]
83) Shimazaki M, Sasaki T, Hikosaka K, Nakashizuka T (2011) Environmental dependence of population dynamics and height growth of a subalpine conifer across its vertical distribution: an approach using high-resolution aerial photographs. Global Change Biology,17: 3431-3438. [Wiley]
84) Sasaki T, Katabuchi M, Kamiyama C, Shimazaki T, Nakashizuka T, Hikosaka K (2012a) Diversity partitioning of moorland plant communities across hierarchical spatial scales. Biodiversity and Conservation, 21: 1577-1588. [Springer]
85) Sasaki T, Katabuchi M, Kamiyama C, Shimazaki T, Nakashizuka T, Hikosaka K (2012b) Nestedness and niche-based species loss in moorland plant communities. Oikos, 121: 1783-1790. [Wiley]
86) Akita R, Kamiyama C, Hikosaka K (2012) Polygonum sachalinense alters the balance between capacities of regeneration and carboxylation of ribulose-1,5-bisphosphate in response to growth CO2 increment but not the nitrogen allocation within the photosynthetic apparatus. Physiologia Plantarum, 146: 404-412. [Wiley]
87) Nagashima H, Hikosaka K (2012) Not only light quality but also mechanical stimuli are involved in height convergence in crowded Chenopodium album stand. New Phytologist, 195: 803-811. [Wiley]
88) Hikosaka K, Anten NPR (2012) An evolutionary game of leaf dynamics and its consequences for canopy structure. Functional Ecology, 26: 1024-1032. [Wiley] [Lay summary]
89) Nagano S, Nakano T, Hikosaka K, Maruta E (2013) Pinus pumila photosynthesis is suppressed by water stress in a wind-exposed mountain site. Arctic, Antarctic and Alpine Research, 45: 229-237. [AAAR]
90) Sasaki T, Katabuchi M, Kamiyama C, Shimazaki M, Nakashizuka T Hikosaka, K (2013) Variations in species composition of moorland plant communities along environmental gradients within a subalpine zone in northern Japan. Wetlands, 33: 269-277. [Springer]
91) Oikawa S, Okada M, Hikosaka K (2013) Effects of elevated CO2 on leaf area dynamics in nodulating and non-nodulating soybean stands. Plant and Soil, 373:627-639. [Springer]
92) Yamori W, Hikosaka K, Way D (2014) Temperature response of photosynthesis in C3, C4 and CAM plants: Temperature acclimation and Temperature adaptation. Photosynthesis Research 119: 101-117. [Springer]
93) Iio A, Hikosaka K, Anten NPR, Nakagawa Y, Ito A (2014) Global dependence of field-observed leaf area index on climate in woody species: Systematic review. Global Ecology and Biogeography, 23: 274-285. [Wiley]
94) Sasaki T, Katabuchi M, Kamiyama C, Shimazaki T, Nakashizuka T, Hikosaka K (2014) Vulnerability of moorland plant communities to environmental change: consequences of realistic species loss on functional diversity. Journal of Applied Ecology, 51: 299-308. [Wiley]
95) Hikosaka K (2014) Optimal nitrogen distribution within a leaf canopy under direct and diffuse light. Plant, Cell and Environment, 37: 2077-2085. [Wiley]
96) Wang QW, Hidema J, Hikosaka K (2014) Is UV-induced DNA damage greater at higher elevation? American Journal of Botany,101: 796-802. [AmerJBot]
97) Kamiyama C, Katabuchi M, Sasaki T, Shimazaki M, Nakashizuka T, Hikosaka K (2014a) Leaf-trait responses to environmental gradients in moorland communities: contribution of intraspecific variation, species replacement and functional group replacement. Ecological Research, 29: 607-617. [Springer]
98) Kamiyama C, Oikawa S, Hikosaka K (2014b) Seasonal change in light partitioning among coexisting species of different functional groups along elevation gradient in subalpine moorlands. New Phytologist, 204: 913-923. [Wiley]
99) Lin Y-S, Medlyn BE, Duursma RA, Prentice IC, Wang H, Baig S, Eamus D, de Dios VR, Mitchell P, Ellsworth DS, de Beeck MO, Wallin G, Uddling J, Tarvainen L, Linderson M-L, Cernusak LA, Nippert JB, Ocheltree TW, Tissue DT, Martin-StPaul NK, Rogers A, Warren JM, DeAngelis P, Hikosaka K, Han Q, Onoda Y, Gimeno TE, Barton CVM, Bennie J, Bonal D, Bosc A, Löw M, Macinins-Ng C, Rey A, Rowland L, Setterfield SA, Tausz-Posch S, Zaragoza-Castells J, Broadmeadow MSJ, Drake JE, Freeman M, Ghannoum O, Hutley LB, Kelly JW, Kikuzawa K, Kolari P, Koyama K, Limousin J-M, Meir P, Lola da Costa AC, Mikkelsen TN, Salinas N, Sun W, Wingate L (2015) Optimal stomatal behaviour around the world. Nature Climate Change, 5: 459-464. [Nature Publishing Group]
100) Noguchi K, Yamori W, Hikosaka K, Terashima I (2015) Homeostasis of the temperature sensitivity of respiration over a range of growth temperatures indicated by a modified Arrhenius model. New Phytologist, 207: 34-42. [Wiley]
101) Kubota S, Iwasaki T, Hanada K, Nagano AJ, Fujiyama A, Toyoda A, Sugano S, Suzuki Y, Hikosaka K, Ito M, Morinaga SI (2015) A genome scan for genes underlying microgeographic-scale local adaptation in a wild Arabidopsis species. PLOS Genetics, e1005361. [PLOS Genetics]
102) Siefert A, Violle C, Chalamandrier L, Albert CH, Taudiere A, Fajardo A, Aarssen LW, Baraloto CB, Carlucci MB, Cianciaruso MV, Dantas VdL, de Bello F, Duarte LDS, Fonseca CR, Freschet GT, Gaucherand S, Gross N, Hikosaka K, Jackson B, Jung V, Kamiyama C, Katabuchi M, Kembel SW, Kchenin E, Kraft NJB, Lagerström A, Le Bagousse-Pinguet, Li Y, Mason N, Messier J, Nakashizuka T, Oberton JMcC, Peltzer D, Pérez-Ramos IM, Pillar VD, Prentice HC, Richardson, Sasaki T, Schamp BS, Schöb C, Shipley B, Sundqvist M, Sykes MT, Vandewalle M, Wardle DA (2015) A global meta-analysis of the relative extent of intraspecific trait variation in plant communities. Ecology Letters, 18: 1406-1419. [Wiley]
103) Oguchi R, Ozaki H, Hanada K. Hikosaka K (2016) Which plant trait explains the variations in relative growth rate and its response to elevated carbon dioxide concentration among Arabidopsis thaliana ecotypes derived from a variety of habitats? Oecologia, 180: 865-876. [Springer]
104) Yamaguchi DP, Nakaji T, Hiura T, Hikosaka K (2016) Effects of seasonal change and experimental warming on the temperature dependence of photosynthesis in the canopy leaves of Quercus serrata. Tree Physiology, 36: 1283-1295. [Oxford]
105) van Loon M, Rietkerk M, Dekker SC, Hikosaka K, Ueda MU, Anten NPR (2016) Plant-plant interactions mediate the plastic and genotypic response of Plantago asiatica to CO2: an experiment with plant populations from naturally high CO2 areas. Annals of Botany, 117: 1197-1207. [Oxford]
106) Hikosaka K, Anten NPR, Borjigidai A, Kamiyama C, Sakai H, Hasegawa T, Oikawa S, Iio A, Watanabe M, Koike T, Nishina K, Ito A (2016) A meta-analysis of leaf nitogen distribution within plant canopies. Annals of Botany, 118: 239-247. [Oxford]
107) Hikosaka K (2016) Optimality of nitrogen distribution among leaves in plant canopies. Journal of Plant Research, 129: 299-311. [Springer]
108) Wang QW, Kamiyama C, Hidema J, Hikosaka K (2016) UV-B induced DNA damage and UV-B tolerance mechanisms in species with different functional groups coexisting in subalpine moorlands. Oecologia, 181: 1069–1082. [Springer]
109) Wang QW, Nagano S, Ozaki H, Morinaga SI, Hidema J, Hikosaka K (2016) Functional differentiation in UV-B-induced DNA damage and growth inhibition between highland and lowland ecotypes of two Arabidopsis species. Environmental and Experimental Botany, 131: 110-119. [ScienceDirect]
110) Ueda MU, Onoda Y, Kamiyama C, Hikosaka K (2017) Decades-long effects of high CO2 concentration on soil nitrogen dynamics in a natural CO2 spring. Ecological Research, 32: 215-225. [Springer]
111) Onoda Y, Wright IJ, Evans JR, Hikosaka K, Kitajima K, Niinemets Ü, Poorter H, Tosens T, Westoby M (2017) Physiological and structural tradeoffs underlying the leaf economics spectrum. New Phytologist, in press.
112) Muryono M, Chen CP, Sakai H, Tokida T, Hasegawa T, Usui Y, Nakamura H, Hikosaka K (2017) Nitrogen distribution in leaf canopies of a high-yielding rice (Oryza sativa L.) cultivar Takanari. Crop Science, in press.
1) Hikosaka K, Terashima I, Katoh S (1992) Effects of light, nutrient and age on nitrogen content and photosynthesis of leaves. In: ed by Murata N, Research in Photosynthesis Vol. IV, pp. 381-384, Kluwer Academic Publishers, Dordrecht.
2) Hikosaka K, Okada K, Terashima I, Katoh S (1993) Acclimation and senescence of leaves: their roles in canopy photosynthesis. In: eds by Yamamoto HY, Smith CM, Photosynthetic Responses to the Environment, pp. 1-13, American Society of Plant Physiologist, Lancaster.
3) Terashima I, Ishibashi M, Ono K, Hikosaka K (1995) Three resistances to CO2 diffusion: leaf-surface water, intercellular spaces and mesophyll cells. In: ed by Mathis P, Photosynthesis: From Light to Biosphere Vol V, pp. 537-542, Kluwer Academic Press, Dordrecht.
4) Hikosaka K, Murakami A, Hirose T (1998b) Temperature acclimation of the photosynthetic apparatus: balancing regeneration and carboxylation of ribulose bisphosphate. In: ed. G. Garab,Photosynthesis: Mechanisms and effects. Vol. V, pp. 3395-3398. Kluwer Academic Press, Dordrecht.
5) Anten NPR, Hikosaka K, Hirose T (2000) Nitrogen utilisation and the photosynthetic system. In: eds. B Marshall and J Roberts, Leaf development and canopy growth. pp. 171-203, Sheffield Acedemic Press, Sheffield.
6) Hikosaka K, Hirose T (2001) Temperature acclimation of the photosynthetic apparatus in an evergreen shrub, Nerium oleander. PS2001 Proceedings: 12th International Congress on Photosynthesis. CSIRO Publishing, Melbourne.
7) Onoda Y, Hikosaka K, Hirose T (2005) The balance between capacities of RuBP carboxylation and RuBP regeneration: Interspecific variation in response to seasonal environment. In: eds. van der Est A, Bruce D. Photosynthesis: Fundamental Aspects to Global Perspectives. pp. 626-628. ACG Publishing, Lawrence.
8) Oguchi R, Hikosaka K, Hiura T, Hirose T (2005) Photosynthetic light acclimation of tree seedlings to artificial gap formations in a cool-temperate deciduous forest. In: eds. van der Est A, Bruce D. Photosynthesis: Fundamental Aspects to Global Perspectives, 628-630. ACG Publishing, Lawrence.
9) Hikosaka K (2005) Nitrogen partitioning in the photosynthetic apparatus of Plantago asiatica leaves acclimated to different temperature and light conditions.In: eds. van der Est A, Bruce D. Photosynthesis: Fundamental Aspects to Global Perspectives, pp. 632-634. ACG Publishing, Lawrence.
10) Muller O, Hikosaka K, Anten NPR, Werger MJA, Hirose T (2005) Optimal leaf nitrogen content of an evergreen understorey plant in a temperate climate. In: eds. van der Est A, Bruce D. Photosynthesis: Fundamental Aspects to Global Perspectives, pp. 636-638. ACG Publishing, Lawrence.
11) Kohyama T, Yoshioka T, Urabe J, Hikosaka K, Sugimoto A, Shibata H, Wada E (2007) Terrestrial ecosystems in Monsoon Asia: scaling up from shoot module to watershed. In: eds, Canadel J, Pataki D, Pitelka L, pp. 285-296, Terrestrial ecosystems in a changing world. Springer-Verlag, Berlin.
12) Hikosaka K, Yasumura Y, Muller O, Oguchi R (2014) Resource allocation and trade-offs in carbon gain of leaves under changing environment. In; eds. Tausz M, Grulke N. Trees in a changing environment. Plant ecophysiology Vol. 9. Springer, Dordrecht. [Springer]
13) Hikosaka K, Niinemets Ü, Anten NPR (2016) Canopy Photosynthesis: From Basics to Applications. Springer, Berlin. [Springer]
14) Hikosaka K, Noguchi K, Terashima I (2016) Modeling leaf gas exchange. In: eds. Hikosaka K, Niinemets Ü, Anten NPR, pp. 61-100, Canopy Photosynthesis: From Basics to Applications. Springer, Berlin. [Springer]
15) Hikosaka K, Kumagai T, Ito A (2016) Modeling canopy photosynthesis. In: eds. Hikosaka K, Niinemets Ü, Anten NPR, pp. 239-268, Canopy Photosynthesis: From Basics to Applications. Springer, Berlin. [Springer]
16) Nakashizuka T, Shimazaki M, Sasaki T, Tanaka T, Kurokawa H, Hikosaka K (2016) Influences of climatic change on the distribution and population dynamics of subalpine coniferous forest in the Hakkoda Mountains, Northern Japan. In: ed. Kudo G, pp. 1-15, Structure and function of mountain ecosystems in Japan.[Springer]
17) Hikosaka K, Sasaki T, Kamiyama C, Katabuchi M, Oikawa S, Shimazaki M, Kimura H, Nakashizuka T (2016) Trait-based approaches for understanding species niche, coexistence and functional diversity in subalpine moorlands. In: ed. Kudo G, pp. 17-40, Structure and function of mountain ecosystems in Japan.[Springer]