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��ࡱ�>��	&(����!"#$%���������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������{�	��Ȟbjbjz�z�	8����(I���������:!:!:!:!:!����N!N!N!8�!<�%|N!�t�>'L/(t/t/t/c0�6<=8 �stttttt$lw�zL%t]:!]9c0c0]9]9%t:!:!t/t/��t�=�=�=]9�:!t/:!t/_a��=]9�s�=�=��I�CKt/������7�%H�����<�JKa�t0�t�J�jz%=�jz(CKCK0jz:!sK�]9]9�=]9]9]9]9]9%t%t�=]9]9]9�t]9]9]9]9��������������������������������������������������������������������jz]9]9]9]9]9]9]9]9]9�  :	Soil temperature and phosphorus supply interactively affect physiological responses of white birch to CO2 elevation

Gabriel Danyagri and Qing-Lai Dang*

Faculty of Natural Resources Management, Lakehead University, 955 Oliver Road, Thunder Bay, Ontario, Canada P7B 5E1

Corresponding author: Qing-Lai Dang
Telephone: (807) 343-8238
Facsimile: (807) 343-8116
E-mail:  HYPERLINK "mailto:qdang@" qdang@lakeheadu.ca







Abstract
We examined how P supply and Tsoil interacted in affecting physiological responses in white birch (Betula papyrifera) to [CO2]. We exposed seedlings to 7, 17 and 27 �C Tsoil, 0.1479, 0.3029 and 0.5847 mM P2O5, and 360 and 720 �mol mol-1 [CO2] for four months. We hypothesized that low Tsoil exacerbate low P effect, leading to greater photosynthetic down-regulation at elevated [CO2].  The CO2 elevation increased photosynthetic rate (Pn) at growth [CO2], but reduced Pn measured at 360 �mol mol-1 CO2 by 55% and this decline was attributed to declines in stomatal conductance. However, gs showed no significant response to [CO2] at low Tsoil or to Tsoil at elevated [CO2].  P supply did not significantly affect Pn. Photosynthetic water-use-efficiency declined with increasing Tsoil under ambient but not elevated [CO2]. Furthermore, CO2 elevation increased IWUE at 17 and 27 but not at 7 �C Tsoil.  At 17 oC, Tsoil, Vcmax and J declined with increasing P under ambient [CO2] but the trend was the opposite under elevated [CO2]. At 7 oC Tsoil, Vcmax and J declined with increasing P at elevated [CO2] but showed no significant response at ambient [CO2].  P effects on triose phosphate utilization varied with Tsoil and [CO2]. 
Additional keywords: Betula  papyrifera Mash, foliar gas exchange, water-use-efficiency, stomatal conductance, Rubisco, boreal trees, climate change.
Introduction
Photosynthetic carbon fixation by trees is the primary contributor to the total productivity of forest ecosystems. A good understanding of how increases in atmospheric CO2 concentration ([CO2]) will affect the photosynthesis of trees will be critical for understanding how climate change will affect the structure, functioning and productivity of forest ecosystems. Photosynthetic responses to CO2 elevations can vary with species, physiological conditions of plants and environmental conditions. For example, CO2 elevations generally result in a down-regulation of photosynthetic capacity in plants that are nutrient-stressed  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_1" \o "Rogers, 1998 #617" 1-8]. Most studies have shown that nutrient deficiency reduces the benefits of CO2 elevation to plants  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_2" \o "Saxe, 1998 #148" 2,  HYPERLINK \l "_ENREF_6" \o "Zhang, 2006 #442" 6,  HYPERLINK \l "_ENREF_7" \o "Long, 2004 #619" 7,  HYPERLINK \l "_ENREF_9" \o "Nowak, 2004 #123" 9]. However, past studies have generally focused on nitrogen because it generally is the most limiting nutrient element to plants on natural sites  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_6" \o "Zhang, 2006 #442" 6,  HYPERLINK \l "_ENREF_8" \o "Cao, 2007 #620" 8,  HYPERLINK \l "_ENREF_10" \o "Li, 2004 #487" 10,  HYPERLINK \l "_ENREF_11" \o "Crous, 2008 #621" 11]. Phosphorus is another key nutrient element that regulates photochemical and biochemical reactions in photosynthesis and is often deficient in natural environments  ADDIN EN.CITE <EndNote><Cite><Author>Lambers</Author><Year>2008</Year><RecNum>417</RecNum><DisplayText>[12]</DisplayText><record><rec-number>417</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">417</key></foreign-keys><ref-type name="Book">6</ref-type><contributors><authors><author>Lambers, Hans</author><author>Chapin III, Stuart F.</author><author>Pons, Thinjs L.</author></authors></contributors><titles><title>Plant physiological eclogy</title></titles><section>540</section><dates><year>2008</year></dates><pub-location>New York</pub-location><publisher>Springer</publisher><urls></urls></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_12" \o "Lambers, 2008 #417" 12]. Phosphorus is often the most limiting or second most limiting element to the aboveground primary productivity of forests  ADDIN EN.CITE <EndNote><Cite><Author>Plassard</Author><Year>2010</Year><RecNum>623</RecNum><DisplayText>[13]</DisplayText><record><rec-number>623</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">623</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Plassard, C.</author><author>Dell, B.</author></authors></contributors><titles><title>Phosphorus nutrition of mycorrhizal trees</title><secondary-title>Tree Physiology</secondary-title></titles><periodical><full-title>Tree Physiology</full-title></periodical><pages>1129-1139</pages><volume>30</volume><number>9</number><dates><year>2010</year><pub-dates><date>September 1, 2010</date></pub-dates></dates><urls><related-urls><url>http://treephys.oxfordjournals.org/content/30/9/1129.abstract</url></related-urls></urls><electronic-resource-num>10.1093/treephys/tpq063</electronic-resource-num></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_13" \o "Plassard, 2010 #623" 13]. However, the effect of P supply on photosynthetic response to CO2 elevation is not well studied. 
Phosphorus is an essential element for some vital structural and metabolic functions of plants and its deficiency can reduce energy transfer and even lead to a breakdown of cell membranes  ADDIN EN.CITE <EndNote><Cite><Author>Oosterhuis</Author><Year>2007</Year><RecNum>624</RecNum><DisplayText>[14]</DisplayText><record><rec-number>624</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">624</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Oosterhuis, D. M.</author><author>Bibi, A. C.</author><author>Gonias, E. D.</author><author>Mozaffari, M.</author></authors></contributors><titles><title>Effect of phosphorus deficiency on cotton physiology. </title><secondary-title>AAES Research Series 562</secondary-title></titles><periodical><full-title>AAES Research Series 562</full-title></periodical><dates><year>2007</year></dates><urls></urls></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_14" \o "Oosterhuis, 2007 #624" 14]. Phosphorus deficiency can limit photosynthesis indirectly by reducing the total leaf area of a plant  ADDIN EN.CITE <EndNote><Cite><Author>Chaudhary</Author><Year>2008</Year><RecNum>625</RecNum><DisplayText>[15]</DisplayText><record><rec-number>625</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">625</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Chaudhary, MuhammadIqbal</author><author>Adu-Gyamfi, JosephJ</author><author>Saneoka, Hirofumi</author><author>Nguyen, NguyenTran</author><author>Suwa, Ryuichi</author><author>Kanai, Shynsuke</author><author>El-Shemy, HanyA</author><author>Lightfoot, DavidA</author><author>Fujita, Kounosuke</author></authors></contributors><titles><title>The effect of phosphorus deficiency on nutrient uptake, nitrogen fixation and photosynthetic rate in mashbean, mungbean and soybean</title><secondary-title>Acta Physiologiae Plantarum</secondary-title><alt-title>Acta Physiol Plant</alt-title></titles><periodical><full-title>Acta Physiologiae Plantarum</full-title><abbr-1>Acta Physiol Plant</abbr-1></periodical><alt-periodical><full-title>Acta Physiologiae Plantarum</full-title><abbr-1>Acta Physiol Plant</abbr-1></alt-periodical><pages>537-544</pages><volume>30</volume><number>4</number><keywords><keyword>BNF</keyword><keyword>Leaf area development</keyword><keyword>Mashbean</keyword><keyword>Mungbean</keyword><keyword>Soybean</keyword><keyword>32P-labelled P</keyword></keywords><dates><year>2008</year><pub-dates><date>2008/07/01</date></pub-dates></dates><publisher>Springer-Verlag</publisher><isbn>0137-5881</isbn><urls><related-urls><url>http://dx.doi.org/10.1007/s11738-008-0152-8</url></related-urls></urls><electronic-resource-num>10.1007/s11738-008-0152-8</electronic-resource-num><language>English</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_15" \o "Chaudhary, 2008 #625" 15], or more directly by reducing Rubisco activity and RuBP regeneration  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_16" \o "Brooks, 1986 #626" 16-19]. Studies using isolated chloroplasts and other in-vitro systems show that phosphorus is involved in the activation of Rubisco  ADDIN EN.CITE <EndNote><Cite><Author>Heldt</Author><Year>1978</Year><RecNum>704</RecNum><DisplayText>[20]</DisplayText><record><rec-number>704</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">704</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Heldt, H.W., </author><author>Chon, C. J.</author><author>Lorimer, G. H. </author></authors></contributors><titles><title>Phosphate requirement for the light activation of ribulosc-1.5-bisphosphate carboxylase in intact spinach chloroplast. </title><secondary-title>FEBS Letters</secondary-title></titles><periodical><full-title>FEBS Letters</full-title></periodical><pages>234 - 240</pages><volume>92</volume><dates><year>1978</year></dates><urls></urls></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_20" \o "Heldt, 1978 #704" 20], the modulation of ribulose-5-phosphate kinase and fructose-l,6-bisphosphate phosphatase  ADDIN EN.CITE <EndNote><Cite><Author>Leegood</Author><Year>1985</Year><RecNum>705</RecNum><DisplayText>[21]</DisplayText><record><rec-number>705</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">705</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Leegood, R. C.</author><author>Walker, D. A.</author><author>Foyer, C. H.</author></authors></contributors><titles><title>Regulation of the Benson�Calvin cycle. pp 189�258 in N. Barber and  R. Barker (eds.) Photosynthetic mechanisms and the environment, Elsevier, Amsterdam.</title></titles><dates><year>1985</year></dates><urls></urls></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_21" \o "Leegood, 1985 #705" 21], the transport of triose-phosphate (TP) across the chloroplast membrane by the Pi-translocator and the regulation of photophosphorylation  ADDIN EN.CITE <EndNote><Cite><Author>Fl�gge</Author><Year>1989</Year><RecNum>706</RecNum><DisplayText>[22]</DisplayText><record><rec-number>706</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">706</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Fl�gge, U. I.,</author><author>Fischer, K.</author><author>Gross, A.</author><author>Sebald, W.</author><author>Lottspeich, F.</author><author>Eckerskorn, C. </author></authors></contributors><titles><title>The triose phosphate-3-phosphoglyceratephosphate translocator from spinach chloroplasts: nucleotide sequence of a full-length cDNA clone and import of the in vitro synthesized precursor protein into chloroplasts</title><secondary-title>EMBO Journal </secondary-title></titles><periodical><full-title>EMBO Journal</full-title></periodical><pages>39 � 46</pages><volume>8</volume><dates><year>1989</year></dates><urls></urls></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_22" \o "Fl�gge, 1989 #706" 22].  ADDIN EN.CITE <EndNote><Cite><Author>Rao</Author><Year>1989</Year><RecNum>707</RecNum><DisplayText>[23]</DisplayText><record><rec-number>707</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">707</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Rao, M.</author><author>Terry, N.</author></authors></contributors><titles><title>Leaf phosphate status, photosynthesis and carbon partitioning in sugar beet. I. Changes in growth, gas exchange and Calvin cycle enzymes</title><secondary-title>Plant Physiol. </secondary-title></titles><periodical><full-title>Plant physiol.</full-title></periodical><pages>814 � 819</pages><volume>90</volume><dates><year>1989</year></dates><urls></urls></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_23" \o "Rao, 1989 #707" 23] have found that a deficiency in inorganic phosphate (Pi) results in a substantial increase in non-stomatal limitation to photosynthesis. All the above physiological processes can affect photosynthetic response to CO2 elevation.  ADDIN EN.CITE <EndNote><Cite><Author>Tissue</Author><Year>2010</Year><RecNum>708</RecNum><DisplayText>[24]</DisplayText><record><rec-number>708</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">708</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Tissue, David T.</author><author>Lewis, James D.</author></authors></contributors><titles><title><style face="normal" font="default" size="100%">Photosynthetic responses of cottonwood seedlings grown in glacial through future atmospheric [CO</style><style face="subscript" font="default" size="100%">2</style><style face="normal" font="default" size="100%">] vary with phosphorus supply</style></title><secondary-title>Tree Physiology</secondary-title></titles><periodical><full-title>Tree Physiology</full-title></periodical><pages>1361-1372</pages><volume>30</volume><number>11</number><dates><year>2010</year><pub-dates><date>November 1, 2010</date></pub-dates></dates><urls><related-urls><url>http://treephys.oxfordjournals.org/content/30/11/1361.abstract</url></related-urls></urls><electronic-resource-num>10.1093/treephys/tpq077</electronic-resource-num></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_24" \o "Tissue, 2010 #708" 24] have demonstrated that P deficiency reduces the positive effect of CO2 elevation on photosynthesis in cottonwood.
Soil temperature (Tsoil) also affects plant responses to CO2 elevations. Low Tsoil reduces root permeability and increases water viscosity, leading to a decrease in shoot water potential (�) and stomatal conductance (gs)  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_5" \o "Zhang, 2005 #476" 5,  HYPERLINK \l "_ENREF_12" \o "Lambers, 2008 #417" 12,  HYPERLINK \l "_ENREF_25" \o "Day, 1991 #308" 25]. Reductions in gs and shoot water potential in turn can affect photosynthetic response to CO2 elevation  ADDIN EN.CITE <EndNote><Cite><Author>Lambers</Author><Year>2008</Year><RecNum>417</RecNum><DisplayText>[5, 12]</DisplayText><record><rec-number>417</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">417</key></foreign-keys><ref-type name="Book">6</ref-type><contributors><authors><author>Lambers, Hans</author><author>Chapin III, Stuart F.</author><author>Pons, Thinjs L.</author></authors></contributors><titles><title>Plant physiological eclogy</title></titles><section>540</section><dates><year>2008</year></dates><pub-location>New York</pub-location><publisher>Springer</publisher><urls></urls></record></Cite><Cite><Author>Zhang</Author><Year>2005</Year><RecNum>476</RecNum><record><rec-number>476</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">476</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Zhang, Shouren</author><author>Dang, Qing-Lai</author></authors></contributors><titles><title><style face="normal" font="default" size="100%">Effects of soil temperature and elevated atmospheric CO</style><style face="subscript" font="default" size="100%">2</style><style face="normal" font="default" size="100%"> concentration on gas exchange, in vivo carboxylation and chlorophyll fluorescence in jack pine and white birch seedlings</style></title><secondary-title>Tree Physiology</secondary-title></titles><periodical><full-title>Tree Physiology</full-title></periodical><pages>523-531</pages><volume>25</volume><number>5</number><dates><year>2005</year><pub-dates><date>May 1, 2005</date></pub-dates></dates><urls><related-urls><url>http://treephys.oxfordjournals.org/content/25/5/523.abstract</url></related-urls></urls><electronic-resource-num>10.1093/treephys/25.5.523</electronic-resource-num></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_5" \o "Zhang, 2005 #476" 5,  HYPERLINK \l "_ENREF_12" \o "Lambers, 2008 #417" 12]. For example, low Tsoil is found to reduce the positive effect of CO2 elevations on photosynthesis in various tree species  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_5" \o "Zhang, 2005 #476" 5,  HYPERLINK \l "_ENREF_26" \o "Gavito, 2001 #96" 26-29]. Low Tsoil can also reduce the synergistic effect of CO2 elevation and high N supply on photosynthesis  ADDIN EN.CITE <EndNote><Cite><Author>Ambebe</Author><Year>2010</Year><RecNum>328</RecNum><DisplayText>[28]</DisplayText><record><rec-number>328</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">328</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Ambebe, Titus Fondo</author><author>Dang, Qing-Lai</author></authors></contributors><titles><title><style face="normal" font="default" size="100%">Low moisture availability reduces the positive effect of increased soil temperature on biomass production of white birch (</style><style face="italic" font="default" size="100%">Betula papyrifera</style><style face="normal" font="default" size="100%">) seedlings in ambient and elevated carbon dioxide concentration</style></title><secondary-title>Nordic Journal of Botany</secondary-title></titles><periodical><full-title>Nordic Journal of Botany</full-title></periodical><pages>104-111</pages><volume>28</volume><number>1</number><dates><year>2010</year></dates><publisher>Blackwell Publishing Ltd</publisher><isbn>1756-1051</isbn><urls><related-urls><url>http://dx.doi.org/10.1111/j.1756-1051.2009.00489.x</url></related-urls></urls><electronic-resource-num>10.1111/j.1756-1051.2009.00489.x</electronic-resource-num></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_28" \o "Ambebe, 2010 #328" 28] and growth  ADDIN EN.CITE <EndNote><Cite><Author>Ambebe</Author><Year>2009</Year><RecNum>290</RecNum><DisplayText>[29]</DisplayText><record><rec-number>290</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">290</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Ambebe, Titus Fondo</author><author>Dang, Qing-Lai</author><author>Marfo, Jacob</author></authors></contributors><titles><title>Low soil temperature reduces the positive effects of high nutrient supply on the growth and biomass of white birch seedlings in ambient and elevated carbon dioxide concentrations</title><secondary-title>Botany</secondary-title></titles><periodical><full-title>Botany</full-title></periodical><pages>905-912</pages><volume>87</volume><number>10</number><dates><year>2009</year><pub-dates><date>2009/10/01</date></pub-dates></dates><publisher>NRC Research Press</publisher><isbn>1916-2790</isbn><urls><related-urls><url>http://dx.doi.org/10.1139/B09-060</url></related-urls></urls><electronic-resource-num>10.1139/b09-060</electronic-resource-num><access-date>2012/04/03</access-date></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_29" \o "Ambebe, 2009 #290" 29].  However, the decline in gs at low Tsoil does not lead to a reduction in photosynthesis in all species  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_30" \o "Teskey, 1983 #709" 30,  HYPERLINK \l "_ENREF_31" \o "Blackman, 1985 #710" 31].  Furthermore, low Tsoil has also been observed to reduce the absorption of mineral nutrients directly and/or indirectly by reducing root growth  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_32" \o "Pastor, 1987 #133" 32-35] or mycorrhizal formation  ADDIN EN.CITE <EndNote><Cite><Author>Domisch</Author><Year>2001</Year><RecNum>712</RecNum><DisplayText>[36]</DisplayText><record><rec-number>712</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">712</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Domisch, Timo</author><author>Fin�r, Leena</author><author>Lehto, Tarja</author></authors></contributors><titles><title><style face="normal" font="default" size="100%">Effects of soil temperature on biomass and carbohydrate allocation in Scots pine (</style><style face="italic" font="default" size="100%">Pinus sylvestris</style><style face="normal" font="default" size="100%">) seedlings at the beginning of the growing season</style></title><secondary-title>Tree Physiology</secondary-title></titles><periodical><full-title>Tree Physiology</full-title></periodical><pages>465-472</pages><volume>21</volume><number>7</number><dates><year>2001</year><pub-dates><date>May 1, 2001</date></pub-dates></dates><urls><related-urls><url>http://treephys.oxfordjournals.org/content/21/7/465.abstract</url></related-urls></urls><electronic-resource-num>10.1093/treephys/21.7.465</electronic-resource-num></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_36" \o "Domisch, 2001 #712" 36]. The availability and absorption of phosphorus are particularly sensitive to soil temperature in the boreal forest where it is primarily absorbed through mycorrhizae because of the immobility of the element  ADDIN EN.CITE <EndNote><Cite><Author>Lambers</Author><Year>2008</Year><RecNum>417</RecNum><DisplayText>[12]</DisplayText><record><rec-number>417</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">417</key></foreign-keys><ref-type name="Book">6</ref-type><contributors><authors><author>Lambers, Hans</author><author>Chapin III, Stuart F.</author><author>Pons, Thinjs L.</author></authors></contributors><titles><title>Plant physiological eclogy</title></titles><section>540</section><dates><year>2008</year></dates><pub-location>New York</pub-location><publisher>Springer</publisher><urls></urls></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_12" \o "Lambers, 2008 #417" 12]. However, it is not clear how P supply and soil temperature will interact in affecting tree�s physiological responses to CO2 elevations. As the global climate change progresses in response to increasing atmospheric [CO2] and other greenhouse gases, changes in Tsoil will be inevitable because of changes in the depth and duration of snow cover, air temperature and the duration of soil freezing  ADDIN EN.CITE <EndNote><Cite><Author>Aphalo</Author><Year>2006</Year><RecNum>713</RecNum><DisplayText>[37]</DisplayText><record><rec-number>713</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">713</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Aphalo, P. J.</author><author>Lahti, M.</author><author>Lehto, T.</author><author>Repo, T.</author><author>Rummukainen, A.</author><author>Mannerkoski, H.</author><author>Fin�r, L. </author></authors></contributors><titles><title>Responses of silver birch saplings to low soil temperature</title><secondary-title>Silva Fennica</secondary-title></titles><periodical><full-title>Silva Fennica</full-title></periodical><pages>429�442</pages><volume>40 </volume><number>3</number><dates><year>2006</year></dates><urls></urls></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_37" \o "Aphalo, 2006 #713" 37]. However, soil warming generally lags behind changes in air temperature. Low Tsoil is prevalent in the boreal forest, particularly at sites with poor drainage and northern and eastern slopes  ADDIN EN.CITE <EndNote><Cite><Author>Gordon</Author><Year>1989</Year><RecNum>714</RecNum><DisplayText>[38, 39]</DisplayText><record><rec-number>714</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">714</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Bonan, Gordon B.</author><author>Shugart, Herman H.</author></authors></contributors><titles><title>Environmental factors and ecological processes in boreal forests</title><secondary-title>Annual Review of Ecology and Systematics</secondary-title></titles><periodical><full-title>Annual Review of Ecology and Systematics</full-title></periodical><pages>1-28</pages><volume>20</volume><dates><year>1989</year></dates><publisher>Annual Reviews</publisher><isbn>00664162</isbn><urls><related-urls><url>http://www.jstor.org/stable/2097082</url></related-urls></urls><electronic-resource-num>10.2307/2097082</electronic-resource-num></record></Cite><Cite><Author>Zasada</Author><Year>1997</Year><RecNum>715</RecNum><record><rec-number>715</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">715</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Zasada, J. C.</author><author>Gordon, A. G.</author><author>Slaughter, C. W.</author><author>Duchesne, L. C. </author></authors></contributors><titles><title>Ecological considerations for the sustainable management of the North American boreal forests. IIASA Interim Report IR-97-024/July 67</title></titles><dates><year>1997</year></dates><urls></urls></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_38" \o "Bonan, 1989 #714" 38,  HYPERLINK \l "_ENREF_39" \o "Zasada, 1997 #715" 39]. The combination of warmer air temperature and cold soil may severely constrain the response of boreal forests to climate change. Low Tsoil may have been a contributing factor to the wide spread damages to boreal trees by unseasonal warm temperatures  ADDIN EN.CITE <EndNote><Cite><Author>Man</Author><Year>2009</Year><RecNum>716</RecNum><DisplayText>[40]</DisplayText><record><rec-number>716</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">716</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Man, R. Z, </author><author>Kayahara, G. J.</author><author>Dang, Q.-L.</author><author>Rice, J. A.</author></authors></contributors><titles><title>A case of severe frost damage prior to budbreak in young conifers in Northeastern Ontario: Consequence of climate change? </title><secondary-title>Forestry Chronicle </secondary-title></titles><periodical><full-title>Forestry Chronicle</full-title></periodical><pages>:453 - 462</pages><volume>85</volume><dates><year>2009</year></dates><urls></urls></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_40" \o "Man, 2009 #716" 40].
A better understanding of the interactive effects of P supply and Tsoil on the physiological responses of trees to CO2 elevations will be critical for predicting the potential responses of boreal forests to climate changes associated with rising atmospheric [CO2]. This study investigates the interactive effects of P supply and soil temperature on the physiological responses of white birch (Betula papyrifera Marsh) to the doubling of atmospheric CO2 concentration. Since low soil temperature restricts P absorption by roots and P deficiency can lead to photosynthetic down regulation at elevated [CO2], we hypothesize that low Tsoil will result in a greater degree of photosynthetic down-regulation under elevated [CO2], particularly when P supply is low.  

Materials and Methods
Plant materials
The experiment was conducted at the Thunder Bay campus of Lakehead University. White birch seeds were germinated in horticultural trays filled with a mixture of peat moss and vermiculite (2:1 by volume). Seedlings of uniform height were transplanted into PVC containers (31.5 cm deep, 11/9.5 cm top/bottom diameter) after 4 weeks of germination and moved to treatment greenhouses as described below. 

Experimental design
The experiment was a split-split-plot design consisting of two CO2 concentrations (360  ambient vs. 720 elevated �mol mol-1, main plot), three levels of P supply (0.1479, 0.3029 and 0.5847 mM P2O5, or 0.2958, 0.6058 and 1.1694 mM P, split-plot) and three Tsoil (7, 17 and 27� C, split-split plot). Nitrogen and potassium concentrations were 221 and 150 mg/L, respectively, in all treatments. There were two independent replications (greenhouses) for each CO2 treatment. There were eight seedlings per treatment combination. The soil temperature control system consisted of a large box with plant pots mounted and sealed to the bottom and each pot had a ��-diameter drainage hole in the middle. Tsoil was regulated by circulating temperature-controlled water in the space between seedling pots within the large box. The box was insulated to minimize the influence of air temperature on Tsoil. Further details on the soil temperature control system can be found in  ADDIN EN.CITE <EndNote><Cite><Author>Cheng</Author><Year>2000</Year><RecNum>15</RecNum><DisplayText>[41]</DisplayText><record><rec-number>15</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">15</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Cheng, Song</author><author>Dang, Qing-Lai</author><author>Cai, Tie-Bo</author></authors></contributors><titles><title>A soil temperature control system for ecological research in greenhouses</title><secondary-title>Journal of Forest Research</secondary-title></titles><pages>205-208</pages><volume>5</volume><number>3</number><keywords><keyword>Biomedical and Life Sciences</keyword></keywords><dates><year>2000</year></dates><publisher>Springer Japan</publisher><isbn>1341-6979</isbn><urls><related-urls><url>http://dx.doi.org/10.1007/BF02762403</url></related-urls></urls><electronic-resource-num>10.1007/bf02762403</electronic-resource-num></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_41" \o "Cheng, 2000 #15" 41]. The day/night temperatures were 20 �26/ 15 �18�C and the photoperiod was 16 hours in all the treatments. All the seedlings were fertilized twice a week.

Gas exchange measurements
Six seedlings per treatment combination were randomly selected for measuring photosynthetic response curves to [CO2] after four months of treatment. The measurements were taken using a CIRAS-1 open gas exchange system with an automatic environment control leaf chamber (PP-Systems, Hitchin Hertfordshire, U.K.) on the first unshaded mature leaf from the top of the seedling (3rd to 5th from the tip). All measurements were taken between 0900 and 1200 hr when gas exchange variables were stable over time. The environmental conditions in the leaf chamber were as follows: 50% RH, 800 � mol m-2s-1 PAR and 26 �C leaf temperature. The A/Ci response was measured at 50, 100, 150, 250, 300, 500, 700, 900 and 1500 �mol mol-1 CO2 concentration. The rate of net photosynthesis at growth [CO2] (Pn) and at a common ambient [CO2] (Pn360), transpiration rate and stomatal conductance (gs) were estimated from the response curve of the relevant parameter to measurement [CO2]. Photosynthetic water use efficiency was calculated as IWUE= Pn/transpiration. The rate of in vivo maximal Rubisco carboxylation (Vcmax), rate of photosynthetic electron transport (J), triose-phosphate utilization (TPU) and mesophyll conductance (gm) were calculated using the A/Ci Curve Fitting Utility version 1.1 developed by Sharkey et al. (2007). 

Leaf nutrient (N, P, K) assays
Total foliar nitrogen was analyzed using the LECO CNS 2000 method  ADDIN EN.CITE <EndNote><Cite><Author>Horneck</Author><Year>1998</Year><RecNum>717</RecNum><DisplayText>[42]</DisplayText><record><rec-number>717</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">717</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Horneck, D. A.</author><author>Miller, R. O. </author></authors></contributors><titles><title>Automated Combustion Method with LECO-CNS. Determination of Total Nitrogen in Plant Tissue pp. 75-83. In Yash P. Kalra (Ed.) Handbook of Reference methods for plant analysis, CRC Press LLC, USA</title></titles><dates><year>1998</year></dates><urls></urls></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_42" \o "Horneck, 1998 #717" 42] and P and K were analyzed using nitric/hydrochloric acid digestion method  ADDIN EN.CITE <EndNote><Cite><Author>Munter</Author><Year>1981</Year><RecNum>718</RecNum><DisplayText>[43, 44]</DisplayText><record><rec-number>718</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">718</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Munter, R. C.</author><author>Grande, R. A.</author></authors></contributors><titles><title>Plant Analysis and soil extracts by ICP-atomic emission spectrometry, Pp. 653-672 In R.M. Barnes (Ed.), Developments in Atomic Plasma Spectrochemical Analysis. Heyden and Son, Ltd., London, England</title></titles><dates><year>1981</year></dates><urls></urls></record></Cite><Cite><Author>Miller</Author><Year>1998</Year><RecNum>719</RecNum><record><rec-number>719</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">719</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Miller, R. A.</author></authors></contributors><titles><title> Nitric-perchloric acid wet digestion in an open vessel, Pp 57-61 In Yash P. Kalra (Ed.), Handbook of Reference methods for plant analysis, CRC Press LLC, USA</title></titles><dates><year>1998</year></dates><urls></urls></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_43" \o "Munter, 1981 #718" 43,  HYPERLINK \l "_ENREF_44" \o "Miller, 1998 #719" 44]. The nutrient concentrations were expressed on the basis of leaf area and leaf mass. Photosynthetic Nitrogen- and P-use efficiencies (hereafter referred to as NUE and PUE, respectively) were calculated by dividing Pn  by the corresponding leaf area-based concentration.   
  
Data analysis
The Analysis of Variance (ANOVA) were conducted using the Data Desk 6.0 statistical package (Data Description, Ithaca, NY) on the original variables (i.e., no data transformation) since tests showed both ANOVA assumptions (i.e., normality and homogeneity) were met. When a factor (Tsoil or P) with more than two levels or an interaction was significant, multiple comparisons were conducted using the Least Square Difference (LSD) method. Because of the relatively small sample size in this study and consequently small degree of freedom for the experiment error in the F test (leading to a larger denominator in F calculation), it is more likely for true treatment effects go undetected (Type II error) (Hicks and Turner 1999, Martin et al. 2010). Therefore we accepted the treatment effect as marginally significant when the   probability was greater than 0.05 but equal to or less than  0.10. .Such a practice is used in Martin et al. 2010 and some other studies where the sample size is small.

Results
Gas exchange    
The CO2 elevation significantly increased Pn  at the growth [CO2] but reduced the photosynthetic rate measured at a common ambient [CO2] (Pn360, Table 1, Fig. 1A). The low Tsoil significantly reduced both Pn and Pn360 but there were no significant differences in either between the intermediate and high Tsoil (Table 1, Figs. 1A & 1B). 
The CO2 elevation significantly reduced gs at the intermediate and high but not at the low Tsoil (Table 1, Fig. 1C). Tsoil had similar effects on gs as it did on Pn and Pn360 under the ambient [CO2] but had no significant effect on gs under the elevated [CO2](Table 1, Figs. 1A-1C).
The photosynthetic water use efficiency (IWUE) decreased with increasing  Tsoil under the ambient  [CO2] but was not significantly influenced by Tsoil under the elevated (Table 1, Fig. 1D).  The CO2 elevation significantly increased IWUE at the intermediate and high but not at the low Tsoil (Fig. 1D, Table 1). 
Soil temperature effects on the mesophyll conductance to CO2 differed between the two CO2 treatments: at the ambient [CO2], gm was the lowest at the low Tsoil while there were no significant differences between the other two Tsoil; at the elevated [CO2], gm was the lowest at the high Tsoil and highest at the intermediate Tsoil (Fig. 2A). The CO2 elevation significantly increased gm at the low Tsoil but had no significant effects at other temperatures (Fig. 2A). The internal to ambient CO2 concentration ratio at growth [CO2] (Ci/Ca) was not significantly affected by any of the treatments (Table 1). 
In vivo biochemical and Rubisco activities
Both Vcmax and J had the highest value at the intermediate Tsoil while there were not significantly differences between the low and high Tsoil at the ambient [CO2] (Table 1, Figs. 2B & 2C). At the elevated [CO2], in contrast, Tsoil did not significantly affect Vcmax but J was significantly lower at the high than at the intermediate Tsoil (Fig. 2C). The CO2 elevation significantly reduced Vcmax only at the intermediate Tsoil and J at both intermediate and high Tsoil (Figs. 2B and 2C). Furthermore, Vcmax generally increased with increasing P supply. Although the P effect appeared to have been affected by [CO2] and Tsoil, the interactions were not statistically significant (Fig. 2B, Table 1). 
The low Tsoil significantly reduced the rate of triose phosphate utilization (TPU) (Table 1, Fig. 2D). TPU generally increased with increasing P supply but the difference between the low and intermediate P levels was not statistically significant (Fig.2D).
Foliar nutrient concentrations and nutrient use-efficiencies
The low Tsoil significantly reduced  leaf K concentrations at the ambient but not elevated [CO2] (Table 2, Figs. 3A & 3B). The CO2 elevation significantly reduced foliar K concentrations at the intermediate and high but not at the  low Tsoil (Figs. 3A & 3B).Mass based foliar K concentration increased with increasing P supply (Fig. 3A).

The low Tsoil significantly reduced both mass based (Pm) and leaf area based P concentration (Pa) under the ambient [CO2] but not under the elevated [CO2] (Table 2, Figs. 3C and 3D). The CO2 elevation significantly reduced both Pm and Pa at the intermediate and high Tsoil but not at the low Tsoil (Figs. 3C and 3D). As with Km, Pm at all three Tsoil and Pa at the intermediate and high Tsoil  increased with increasing P supply (Figs. 3C & 3D).; The low Tsoil decreased Pm  at all three P levels (Fig. 3C) while it reduced Pa only in the high P treatment (Fig. 3D). 
 Nm generally increased with increasing P supply under the ambient [CO2] and high Tsoil while there was no clear trend in other treatment combinations (Table 2, Fig. 3E). The CO2 elevation generally decreased Nm with some minor variations with P and Tsoil (no clear patterns, Fig. 3E).  The effects of Tsoil also varied with [CO2] and P levels but did not show clear general patterns except the low Tsoil reduced Nm at the low P level under elevated [CO2] (Fig. 3E). Na was the highest at low P and lowest at the high P under the low Tsoil but the trend was the opposite at other Tsoil Table 2, Fig. 3F). The CO2 elevation significantly reduced Na (Table 2, Fig. 3F). 
The CO2 elevation significantly increased both photosynthetic phosphorus use-efficiency (PUE) and photosynthetic nitrogen use-efficiency (NUE) (Table 2, Figs. 3G and 3H). The low Tsoil significantly reduced the NUE (Table 2, Fig 3H).

Discussion
Photosynthetic measurements at a common CO2 concentration (360 �mol mol-1) suggest that both the low Tsoil and CO2 elevation caused a down-regulation of photosynthesis, but mechanisms responsible for the down regulation were influenced by interactions between soil temperature and CO2.  Under the ambient [CO2], the low Tsoil-induced decline in Pn360 was associated with declines in both stomatal conductance and mesophyll capacity (as indicated by gm, Vcmax and J). Under the elevated [CO2], however, the decline in mesophyll conductance was the primary contributing factor for the decline in Pn360 at the low Tsoil. Furthermore, the sink strength, as indicated by the rate of triose phosphate utilization, contributed to the decline in Pn360 in both CO2 treatments. The declines in both stomatal conductance and parameters describing biochemical and photochemical capacities were responsible for the CO2 elevation induced decline in Pn360, particularly at the intermediate and high soil temperatures.   
Low Tsoil effects on gas exchange are generally more complicated, involving interactions between below-ground and above-ground parts of the plant  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_5" \o "Zhang, 2005 #476" 5,  HYPERLINK \l "_ENREF_12" \o "Lambers, 2008 #417" 12,  HYPERLINK \l "_ENREF_25" \o "Day, 1991 #308" 25]. Larger sample sizes and more comprehensive diagnostic measurements including additional characteristics (such as chlorophyll fluorescence parameters, analyses of water relations) may be necessary to discern the physiological mechanisms governing changes in photosynthesis in response to the above two situations.  Regardless of the mechanisms, the photosynthetic acclimation to elevated CO2 was partial since the photosynthetic rates measured under the corresponding growth CO2 concentration were significantly greater under the elevated than ambient CO2 concentration. A complete acclimation would have resulted in a photosynthetic rate at the elevated [CO2] being equal to that at the ambient [CO2].
Different indictors of photosynthetic down regulation give mixed results in this study. Photosynthetic down regulation is assessed using several different variables in the literature.  The maximum rate of Rubisco carboxylation (Vcmax) and maximum rate of photosynthetic electron transport (J) are often used to indicate changes in the biochemical capacity and photochemical capacity of photosynthetic machinery  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_2" \o "Saxe, 1998 #148" 2,  HYPERLINK \l "_ENREF_5" \o "Zhang, 2005 #476" 5,  HYPERLINK \l "_ENREF_7" \o "Long, 2004 #619" 7,  HYPERLINK \l "_ENREF_45" \o "Ambebe, 2010 #424" 45,  HYPERLINK \l "_ENREF_46" \o "Crous, 2010 #622" 46]. Although there was a decline in both parameters associated with the low soil temperature under the ambient CO2 in this study, it was not the case under elevated CO2, nor was there a decline in them in response to the CO2 elevation. Pn360 is often used as an indicator of the integrated acclimation of photosynthetic capacity and stomatal conductance  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_8" \o "Cao, 2007 #620" 8,  HYPERLINK \l "_ENREF_46" \o "Crous, 2010 #622" 46,  HYPERLINK \l "_ENREF_47" \o "Ro, 2001 #720" 47]. To a certain degree, differences in Pn360 reflect a shift in both the supply function and demand function of photosynthesis  ADDIN EN.CITE <EndNote><Cite><Author>Lambers</Author><Year>2008</Year><RecNum>417</RecNum><DisplayText>[12]</DisplayText><record><rec-number>417</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">417</key></foreign-keys><ref-type name="Book">6</ref-type><contributors><authors><author>Lambers, Hans</author><author>Chapin III, Stuart F.</author><author>Pons, Thinjs L.</author></authors></contributors><titles><title>Plant physiological eclogy</title></titles><section>540</section><dates><year>2008</year></dates><pub-location>New York</pub-location><publisher>Springer</publisher><urls></urls></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_12" \o "Lambers, 2008 #417" 12]. However, as discussed previously, the changes in Pn360 in this study primarily reflect changes in the supply function, i.e., the effects of stomatal conductance. These results suggest that Pn360 can be used to indicate the magnitude of photosynthetic down regulation but not the mechanisms responsible for the down regulation unless it is considered in conjunction with other parameters. Furthermore, Pn360 will not be of any use for predicting photosynthetic performance under a future climate with a doubled atmospheric CO2 concentration because plants will not likely experience the present atmospheric CO2 concentration in the future once the CO2 concentration in the atmosphere is doubled.
The data suggest that white birch will likely have higher water use efficiency in the future under elevated atmospheric CO2 concentration, particularly under warmer soil temperatures. The significant increase in photosynthetic rate and simultaneous decline in stomatal conductance both contributed to the increase in water use efficiency under the elevated CO2. However, such changes did not occur at the low soil temperature. In fact, at the ambient CO2 concentration, water use efficiency declined with increasing soil temperature. At the elevated CO2, in contrast, WUE at warmer soil temperatures (17 and 27 oC) was as high as that at the low soil temperature (7 oC).  These results suggest that the photosynthesis of white birch can be increased by creating warmer soil temperatures in the future without the risk of losing water use efficiency, which occurred under the ambient CO2 concentration. While the soil temperature will most likely increase as the global air temperature increases, further increases in soil temperature can be achieved through silvicultural means, such as site preparation  ADDIN EN.CITE <EndNote><Cite><Author>Orlander</Author><Year>1990</Year><RecNum>721</RecNum><DisplayText>[48]</DisplayText><record><rec-number>721</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">721</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Orlander, G.</author><author>Gemmel, P.</author><author>Hunt, J. </author></authors></contributors><titles><title>Site Preparation: A Swedish Overview. Government of Canada, Province of British Columbia, p. 62</title></titles><dates><year>1990</year></dates><urls></urls></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_48" \o "Orlander, 1990 #721" 48] and manipulation of canopy coverage  ADDIN EN.CITE <EndNote><Cite><Author>Smith</Author><Year>1997</Year><RecNum>722</RecNum><DisplayText>[49]</DisplayText><record><rec-number>722</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">722</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Smith, D.M.</author><author>Larson, B. C. </author><author>Kelty, M. J.</author><author>Ashton, P. M. S. </author></authors></contributors><titles><title>The practice of silviculture- Applied forest ecology,  Nineth Edition. John Wiley and Sons, New York</title></titles><dates><year>1997</year></dates><urls></urls></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_49" \o "Smith, 1997 #722" 49] and soil moisture  ADDIN EN.CITE <EndNote><Cite><Author>Bonan</Author><Year>1989</Year><RecNum>714</RecNum><DisplayText>[38]</DisplayText><record><rec-number>714</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">714</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Bonan, Gordon B.</author><author>Shugart, Herman H.</author></authors></contributors><titles><title>Environmental factors and ecological processes in boreal forests</title><secondary-title>Annual Review of Ecology and Systematics</secondary-title></titles><periodical><full-title>Annual Review of Ecology and Systematics</full-title></periodical><pages>1-28</pages><volume>20</volume><dates><year>1989</year></dates><publisher>Annual Reviews</publisher><isbn>00664162</isbn><urls><related-urls><url>http://www.jstor.org/stable/2097082</url></related-urls></urls><electronic-resource-num>10.2307/2097082</electronic-resource-num></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_38" \o "Bonan, 1989 #714" 38]. The lack of significant responses in stomatal conductance to the CO2 elevation under the adverse soil temperature (i.e., 7 oC) could be interpreted as that the stomatal conductance at this low soil temperature was already at such a low level that it could not go down any further.
Our results demonstrate that whether there is a tradeoff between water use efficiency and nutrient use efficiency depends on the driving factor or factors that cause changes in resource use efficiencies. Generally there is a tradeoff between water use efficiency and nutrient use efficiency  ADDIN EN.CITE <EndNote><Cite><Author>Lambers</Author><Year>2008</Year><RecNum>417</RecNum><DisplayText>[12]</DisplayText><record><rec-number>417</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">417</key></foreign-keys><ref-type name="Book">6</ref-type><contributors><authors><author>Lambers, Hans</author><author>Chapin III, Stuart F.</author><author>Pons, Thinjs L.</author></authors></contributors><titles><title>Plant physiological eclogy</title></titles><section>540</section><dates><year>2008</year></dates><pub-location>New York</pub-location><publisher>Springer</publisher><urls></urls></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_12" \o "Lambers, 2008 #417" 12]. Such a tradeoff exists because within the normal operating range of internal CO2 concentration an increase in stomatal conductance will lead a linear increase in transpiration rate but a curvilinear (thus smaller) increase in photosynthesis, leading to a decrease in water use efficiency (ratio of photosynthesis to transpiration). On the other hand, any increase in photosynthesis will result in an increase in nutrient use efficiency since nutrient concentrations in the leave are constant over a short period of time  ADDIN EN.CITE <EndNote><Cite><Author>Lambers</Author><Year>2008</Year><RecNum>417</RecNum><DisplayText>[12]</DisplayText><record><rec-number>417</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">417</key></foreign-keys><ref-type name="Book">6</ref-type><contributors><authors><author>Lambers, Hans</author><author>Chapin III, Stuart F.</author><author>Pons, Thinjs L.</author></authors></contributors><titles><title>Plant physiological eclogy</title></titles><section>540</section><dates><year>2008</year></dates><pub-location>New York</pub-location><publisher>Springer</publisher><urls></urls></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_12" \o "Lambers, 2008 #417" 12]. Physiological acclimation will complicate the issue. In this study, the low soil temperature increased water use efficiency and decreased nitrogen use efficiency under the ambient CO2 concentration. Under the elevated CO2, in contrast, the low soil temperature decreased nitrogen use efficiency without a corresponding increase in water use efficiency. Furthermore, the CO2 elevation increased both nitrogen use efficiency and water use efficiency. 
The results do not support our hypothesis that the degree of photosynthetic down-regulation in response to CO2 elevation would be greater under low Tsoil and low P supply. The hypothesis was based on the argument that the low Tsoil would suppress the uptake of phosphorus and the resulting lower P concentration in the foliage would in turn exacerbate the photosynthetic down regulation induced by CO2 elevation because of low availability of inorganic phosphorus for the Kelvin Cycle of photosynthesis  ADDIN EN.CITE <EndNote><Cite><Author>Lambers</Author><Year>2008</Year><RecNum>417</RecNum><DisplayText>[12]</DisplayText><record><rec-number>417</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">417</key></foreign-keys><ref-type name="Book">6</ref-type><contributors><authors><author>Lambers, Hans</author><author>Chapin III, Stuart F.</author><author>Pons, Thinjs L.</author></authors></contributors><titles><title>Plant physiological eclogy</title></titles><section>540</section><dates><year>2008</year></dates><pub-location>New York</pub-location><publisher>Springer</publisher><urls></urls></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_12" \o "Lambers, 2008 #417" 12]. However, the basis for the hypothesis did not hold in this study. While there was indeed a significant interaction between soil temperature and phosphorus supply on leaf area based P concentration, soil temperature did not significantly affect foliar P in the low P treatment. Furthermore, P supply did not significantly affect foliage P in the low soil temperature treatment. Therefore, it is not surprising that the indicators for photosynthetic down regulation did not vary in the way proposed in the hypothesis.  
Our results are in contrast to the findings of  ADDIN EN.CITE <EndNote><Cite><Author>Tissue</Author><Year>2010</Year><RecNum>708</RecNum><DisplayText>[24]</DisplayText><record><rec-number>708</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">708</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Tissue, David T.</author><author>Lewis, James D.</author></authors></contributors><titles><title><style face="normal" font="default" size="100%">Photosynthetic responses of cottonwood seedlings grown in glacial through future atmospheric [CO</style><style face="subscript" font="default" size="100%">2</style><style face="normal" font="default" size="100%">] vary with phosphorus supply</style></title><secondary-title>Tree Physiology</secondary-title></titles><periodical><full-title>Tree Physiology</full-title></periodical><pages>1361-1372</pages><volume>30</volume><number>11</number><dates><year>2010</year><pub-dates><date>November 1, 2010</date></pub-dates></dates><urls><related-urls><url>http://treephys.oxfordjournals.org/content/30/11/1361.abstract</url></related-urls></urls><electronic-resource-num>10.1093/treephys/tpq077</electronic-resource-num></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_24" \o "Tissue, 2010 #708" 24] where the positive effect of CO2 elevation on light saturated rate of photosynthesis in cottonwood diminished with decreasing P supply. There are several explanations for the differences. Firstly, it is possible that different species respond differently. Secondly, the range of P supply was different between the two studies. While the P level in the high P treatment of  ADDIN EN.CITE <EndNote><Cite><Author>Tissue</Author><Year>2010</Year><RecNum>708</RecNum><DisplayText>[24]</DisplayText><record><rec-number>708</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">708</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Tissue, David T.</author><author>Lewis, James D.</author></authors></contributors><titles><title><style face="normal" font="default" size="100%">Photosynthetic responses of cottonwood seedlings grown in glacial through future atmospheric [CO</style><style face="subscript" font="default" size="100%">2</style><style face="normal" font="default" size="100%">] vary with phosphorus supply</style></title><secondary-title>Tree Physiology</secondary-title></titles><periodical><full-title>Tree Physiology</full-title></periodical><pages>1361-1372</pages><volume>30</volume><number>11</number><dates><year>2010</year><pub-dates><date>November 1, 2010</date></pub-dates></dates><urls><related-urls><url>http://treephys.oxfordjournals.org/content/30/11/1361.abstract</url></related-urls></urls><electronic-resource-num>10.1093/treephys/tpq077</electronic-resource-num></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_24" \o "Tissue, 2010 #708" 24] was comparable to ours (0.50 vs. 0.58 mM P2O5), their low P supply was much lower than ours (0.004 vs. 0.15 mM P2O5).  Therefore, it is possible that the low P level in this study was not low enough to test the effect of P stress and its interaction with soil temperature. Thirdly, the effect of P supply may have been manifested in different traits in the two species. There are several mechanisms by which P deficits can limit the physiology and growth of plants, including the biochemical capacity of photosynthesis and total leaf area per plant. The low P supply in this study indeed resulted in a significantly smaller-sized leaves and smaller amount of leaves per tree  ADDIN EN.CITE <EndNote><Cite><Author>Ambebe</Author><Year>2012</Year><RecNum>322</RecNum><DisplayText>[50]</DisplayText><record><rec-number>322</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">322</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Ambebe, Titus F.</author><author>Danyagri, Gabriel</author><author>Dang, Qing-Lai</author></authors></contributors><titles><title><style face="normal" font="default" size="100%">Low soil temperature inhibits the stimulatory effect of elevated [CO</style><style face="subscript" font="default" size="100%">2</style><style face="normal" font="default" size="100%">] on height and biomass accumulation of white birch seedlings grown under three non-limiting phosphorus conditions (</style><style face="italic" font="default" size="100%">in press</style><style face="normal" font="default" size="100%">)</style></title><secondary-title>Nordic Journal of Botany</secondary-title></titles><periodical><full-title>Nordic Journal of Botany</full-title></periodical><dates><year>2012</year></dates><urls></urls></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_50" \o "Ambebe, 2012 #322" 50], indicating a different strategy that the species uses in coping with low P supply than that assumed in our hypothesis, which is in contrast to the strategy used by some other tree species, such as cottonwood  ADDIN EN.CITE <EndNote><Cite><Author>Tissue</Author><Year>2010</Year><RecNum>708</RecNum><DisplayText>[24]</DisplayText><record><rec-number>708</rec-number><foreign-keys><key app="EN" db-id="rvertsx582eeznewfrpxfxzwx9s0pv2s9p5p">708</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Tissue, David T.</author><author>Lewis, James D.</author></authors></contributors><titles><title><style face="normal" font="default" size="100%">Photosynthetic responses of cottonwood seedlings grown in glacial through future atmospheric [CO</style><style face="subscript" font="default" size="100%">2</style><style face="normal" font="default" size="100%">] vary with phosphorus supply</style></title><secondary-title>Tree Physiology</secondary-title></titles><periodical><full-title>Tree Physiology</full-title></periodical><pages>1361-1372</pages><volume>30</volume><number>11</number><dates><year>2010</year><pub-dates><date>November 1, 2010</date></pub-dates></dates><urls><related-urls><url>http://treephys.oxfordjournals.org/content/30/11/1361.abstract</url></related-urls></urls><electronic-resource-num>10.1093/treephys/tpq077</electronic-resource-num></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_24" \o "Tissue, 2010 #708" 24].
This study has shown some complicated interactions among soil temperature, nutrient supply and ratios of different nutrient elements. For instance, the CO2 elevation reduced Ka and Pa only at the intermediate and high soil temperature while it resulted in lower Na at all three soil temperatures. Increasing phosphorus supply increased Km but the response of Na showed different patterns at each of the three soil temperatures. These results demonstrate the complicated nature of interactions among nutrient absorption, allocation, physiological functions and their impact on physiological responses to CO2 elevations under different nutrient regimes. Interactions among several factors are much more difficult to study than the main effects of one or two factors and that probably explains the lack of such data in the scientific literature. However, our data show that such interactions in the real world situations can throw the results of studies with simple designs out of context or relevance under certain circumstances. Of course studies involving one or two treatment factors are very important for understanding the mechanisms of their effects. However, the interactive effects of multiple factors are probably more important for making more realistic predictions of plant responses and therefore warrant more attention in future research. Furthermore, interactions involving more than two factors are difficult to visualize and present. There is an urgent need to develop new techniques or to adopt techniques that are currently not being used in plant ecophysiology for analyzing and presenting the results of studies with multiple treatments. Common or standardized expressions of interactive effects should facilitate the comparison of different studies and the utilization of results in further efforts such as modeling and predicting whole plant or ecosystem responses to climate changes.
Acknowledgments
We appreciate the technical support of Joan Lee, the Lakehead University Greenhouse Manager, during the course of the experiment.
Funding
This research was supported by National Science and Engineering Research Council, Canada Foundation for Innovation and Ontario Innovation Trusts grants to Q.L. Dang and Lakehead University Graduate Assistantship to G. Danyagri.
 ADDIN EN.REFLIST References

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Tables
Table 1. Probabilities from ANOVA for the effects of soil temperature (Tsoil), phosphorus supply (P) and [CO2] on net photosynthetic rate at growth [CO2] (Pn), photosynthetic rate measured at a common [CO2] (Pn360), stomatal conductance to water (gs), instantaneous water-use-efficiency (IWUE), mesophyll conductance to CO2 (gm), intercellular/atmospheric [CO2] ratio at the growth [CO2] (Ci/Ca), maximum rate of carboxylation (Vcmax), rate of photosynthetic electron transport (J) and triosephosphate utilization (TPU)  in white birch seedlings. The seedlings were grown at 360 and 720 �mol mol-1 [CO2]; 7, 17 and 27� C Tsoil and 241, 493 and 951 mg/L P supply. 
Source of variationCO2TsoilCO2�TsoilPCO2 �PTsoil �PCO2�Tsoil�PPn0.01840.00840.94290.41290.85920.8730.6331Pn360< 0.00010.02580.22460.49500.99300.92090.9887gs0.00910.01030.06520.98890.88450.99180.9492IWUE0.00120.03060.08250.95120.99210.98260.8020gm0.74400.00080.01770.96880.92330.41050.9202Ci/Ca0.19640.54600.42020.91880.46340.46630.8509Vcmax0.06200.13210.05840.07330.24270.41410.5745J0.14570.00020.03990.17550.58230.21220.6157TPU0.1096d"0.00010.12090.02860.30360.49610.4485Table 2. Probabilities from ANOVA for the  effects of Tsoil, P supply and [CO2] on mass-based leaf potassium concentration (Km), area-based leaf potassium concentration (Ka ), mass-based leaf phosphorus concentration (Pm), area-based leaf phosphorus concentration (Pa), mass-based leaf nitrogen concentration (Nm), area-based leaf nitrogen concentration (Na), photosynthetic phosphorus use-efficiency (PUE), nitrogen use efficiency (NUE) and total leaf area per seedling in white birch. Other explanations are as in Table 1.
Source of variationCO2TsoilCO2�TsoilPCO2 �PTsoil �PCO2�Tsoil�PKm<0.00010.09670.00640.00020.26530.66050.6798Ka0.03290.12650.09560.12150.38770.13490.9885Pm0.01600.00030.0618<0.00010.16490.33630.4456Pa0.14100.00120.1046<0.00010.13780.03160.6929Nm<0.00010.02340.32680.17560.05480.11370.0609Na0.00140.63670.74790.72490.46440.02710.5478PUE0.02180.24740.21090.17730.97430.72950.9954NUE0.00510.01460.57920.28630.42050.31700.7479
 
Figure captions
Figure 1. Effects of CO2 concentration and soil temperature (Tsoil) on the rate of net photosynthesis at growth CO2 (Pn) and the rate measured at a common ambient CO2 concentration (Pn360), stomatal conductance to water (gs) and instantaneous water-use-efficiency (IWUE) (mean + SE, n= 6) in white birch seedlings. The seedlings were grown under two [CO2] (360 and 720 �mol mol-1), three Tsoil (7, 17 and 27� C) and 3 levels of P supply (0.1479, 0.3029 and 0.5847 mM P2O5). Means with the same letter(s) are not significantly different from one another (P>0.10). Only significant treatments were labeled. Tsoil effects are labeled on the side of the ambient [CO2] since there were no significant interactions between CO2 and Tsoil (P>0.10). ***: p d" 0.01; **: 0.01 < p d" 0.05; *: 0.05< P d" 0.10.  
Figure 2. Effects of CO2, Tsoil and P on mesophyll conductance to CO2 (gm)maximum rate of carboxylation (Vcmax), rate of photosynthetic electron transport (J) a&45<hjstu�������		
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Figure 3. Effects of CO2, Tsoil and P on foliar nutrient concentrations and photosynthetic N and P use efficiency in white birch seedlings. Non-significant effects were pooled in Figures B, G and H to provide a clearer presentation of significant effects. In Figure D, upper case letters indicate Tsoil x P interactions while lower case letters are for CO2 x Tsoil interactions. Other explanations are as in Figures 1 and 2.









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