Evolutionary model of C 4 photosynthesis in genus Flaveria Key words: C 4 photosynthesis, evolution, genus Flaveria,

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1 Flaveria C Evolutionary model of C 4 photosynthesis in genus Flaveria Key words: C 4 photosynthesis, evolution, genus Flaveria, Yuri N. Munekage & Yukimi Y. Taniguchi Graduate School of Biological Sciences, Nara Institute of Science and Technology Takayama, Ikoma, Nara , Japan - C 4 C 3 S H CO 2 C 4 S C 4 T S N CO 2 T C 4 T G N X T CO 2 A G T HN C 3 X CO 2 X C 4 X CO 2 AT C 3 X S T CO 2 S 1,5- / RuBisCO C 4 T A G S C 3 T X S A A C 4 T X AT N C 4 X CO 2 A T C 3 X C(Long 1999) X 19 X N 7500 C 4 A X M 66 C 3 HN S (Sage 2012) N C 3 -C 4 X G A 21 H 12 X S C 3 -C 4 C 4 A A G S (Christin et al. 2011, Sage et al. 2011) C 4 C 3 -C 4 S HN S C 3 -C 4 T T IN T CO 2 X S CO 2 T C 4 X S CO 2 C 3 -C 4 T C 4 A G S T Flaveria X C 3 C 4 ET C C 3 -C 4 C 4 A X C I T 9 A Y. N. Munekage & Y. Y. Taniguchi-1

2 T Flaveria H X C 4 T X S Flaveria C 4 A X HN 3300 T G S Sage et al X H Flaveria C 4 X HC 300 X HN G S Christin et al Flaveria C o X HS C 3 C 4 S 23 A G S Powell 1978, McKown et al X C 3 T G Clade A Clade B X G T 9A X HN 8 1 N Flaveria T C 3 C 3 -C 4 A HN 2 Clade X S C 4 A A (McKown et al Clade A X C 3 -C 4, C 4 C 4 A X H Clade B T C 4 HN C 4 F. brownii T C 3 C 4 T M A CO 2 X O 2 inhibition, % X S E S C 3 50 µl/l, C 3 -C µl/l, C µl/l C 4 5 µl/l CO 2 Ku et al N H C 3 -C 4 C 4 X S M C 4 E C 4 X X S 9T Kranz Flaveria X S C 3 C 4 T A G X H C 3 -C 4 C 4 A G 2 C 4 H Flaveria C 3 T A X H C 3 -C 4 T C C 4 C 4 T C S 3, Mckwon & Dengler 2007 T G N X T A G S Dengler and Nelson 1999 Flaveria T C 3 C 3 -C 4 C 4 T X A HS A Y. N. Munekage & Y. Y. Taniguchi-2

3 C 4 T X Kranz A G Kranz T A X HS A C X (M)A (BS)X HS X T G vein-bs-m-m-bs-vein X S GA H M A X H N X G A Dengler and Nelson 1999 T X N vein-bs-m-m-bs-vein H A HN A Flavera C 3 T X HS G A C 3 -C 4 T I GT C 4 C 4 T A C A X HS A 4 N C 3 -C 4 T C 3 HS o A H M C X G C 4 C 4 T X E AG X G 4 Nakamura et al C 3 -C 4 X E N X H S 5 59 C 4 C 3 -C 4 T C 3 X RuBisCO A H C 3 A S C 3 -C 4 T X CO 2 A CN C 3 CO 2 A G S Bauwe 2011, Keerberg et al T RuBisCO X IN M T X CO 2 A G 5 o X H ot G N CO 2 A C T X IN X C 3 C 3 -C 4 A G T G S ot GDC A X Y. N. Munekage & Y. Y. Taniguchi-3

4 G X S Engelmann et al. 2008, Sage et al X N C 3 -C 4 T X T A G N C 3 -C 4 X C 4 A G S A Flavera N A X S C 3 -C 4 C C 4 N A G S Bauwe 2011 A Flavera C 3 -C 4 T 14 CO 2 C 4 A T G S Monson et al N Flavera C 3 -C 4 T C 4 T C PEPC PPDK NADP- NADP-ME o o A C 3 HS A G S Mallmann et al X S C 4 N A X G Mallmann T X G o o N X C 4 A N HS X RuBisCO A X C 4 F. brownii T X C 4 A C A G S Cheng et al. 1988, Monson et al. 1988, Shulze et al. 2013, Sage 2014 X HN CO 2 C 4 X CO 2 X HN A C 4 C 4 X ET C M A N G A N C 3 -C 4 C 4 C 4 T X Taniguchi et al. in preparation Flaveria X PEPC A 6 A M PPCA A C 3 C 3 -C 4 C 4 C 4 X S X PPCA C 3 -C 4 F. floridana T T HS X H C 4 F. brownii T PPCA T C T Taniguchi et al. in preparation N C 4 Flaveria T PPCA X X G PPCA PPCA X MEM1 A A G N Akyildiz et al H H A Clade B X F. floridana F. brownii T MEM1 X A C N F 2 N PPCA X A H A N Munekage et al. in preparation S PPCA Y. N. Munekage & Y. Y. Taniguchi-4

5 X S G N PEPC ET C PPDK, NADP-ME mrna T G C 4 T A G Taniguchi et al. in preparation C 4 A G C 4 A C A G S A A C 4 T 6 RuBisCO N X G A Flaveria X S Moore et al. 1988, Moore et al C 3 -C 4 T RuBisCO T X H C 4 T T A C G C 4 T X G RuBisCO A X G T T A G CO 2 C 4 A 6 RuBisCO X T X G RBCS X G RBCL A A S Patel and Berry 2008 C 4 Flaveria bidentis T RBCS 5 UTR 3 UTR A X C A G S Patel et al Flaveria 9 X S RBCS X G S A G S M X H X X G N X UTRs N mrna T A T C 4 CO 2 HN X C 3 C M N X 1 CO 2 X C 3 T 3 ATP 2 NADPH A T X H C 4 T 5 ATP 2 NADPH A T ATP N X A A G N Kanai and Edwards 1999 Flaveria T C 4 A HS C 4 C 4 T X C N C 4 F. palmeri C 4 T A C H II A A 7 Nakamura et al T ATP NADPH A G X ATP Y. N. Munekage & Y. Y. Taniguchi-5

6 X A G T C 4 X A N N H C 4 Flaveria T PEPC X G N Ao G o A A G S Moore and Edwards 1986, Meister et al To X NADPH A T N HS C 4 Flaveria T X HS K II A G S A C A G S Meister et al X HS E A S 1 ) X N T G S A X HS C T G N T S) ) A HS HS G N A A X X S C A HS M HS X T X ) X E 9 A X T A T A T HN 1 32.( S HN Akyildiz M, Gowik U, Engelmann S, Koczor M, Streubel M, Westhoff P Evolution and function of a cis-regulatory module for mesophyll-specific gene expression in the C 4 dicot Flaveria trinervia. Plant Cell. 19: Bauwe H Photorespiration: the bridge to C 4 photosynthesis. In: Raghavendra AS, Sage RF, eds. C 4 photosynthesis and related CO 2 concentrating mechanisms. Dordrecht, The Netherlands: Springer, Christin P-A, Osborne CP, Sage RF, Arakaki M, Edwards EJ C 4 eudicots are not younger than C 4 monocots. J Exp Bot 62: Cheng SH, Moore BD, Edwards GE, Ku MS Photosynthesis in Flaveria brownii, a C 4- like Species. Leaf anatomy, characteristics of CO 2 exchange, compartmentation of photosynthetic enzymes, and metabolism of 14 CO 2. Plant Physiology 87: Dengler NG and Nelson T Leaf structure and development in C 4 plants. In: Sage RF, Monson RK, eds. C 4 Plant Biology. San Diego, USA: Academic Press, Engelmann S, Wiludda C, Burscheidt J, Gowik U, Schlue U, Koczor M, Streubel M, Cossu R, Bauwe Y. N. Munekage & Y. Y. Taniguchi-6

7 H, Westhoff P The gene for the P-subunit of glycine decarboxylase from the C 4 species Flaveria trinervia: analysis of transcriptional control in transgenic Flaveria bidentis (C 4 ) and Arabidopsis (C 3 ). Plant Physiol, 146: Kanai R, Edwards GE The biochemistry of C 4 photosynthesis. In: Sage RF, Monson RK, eds. C 4 Plant Biology. San Diego, USA: Academic Press, Keerberg O, Pärnik T, Ivanova H, Bassüner B, Bauwe H C 2 photosynthesis generates about 3-fold elevated leaf CO 2 levels in the C 3 -C 4 intermediate species Flaveria pubescens. J Exp Bot 65: Ku MSB, Wu J, Dai Z, Scott RA, Chu C, Edward GE Photosynthetic and photorespiratory characteristics of Flaveria species. Plant Physiology 96: Long SP Environmental Responses. In: Sage RF, Monson RK, eds. C 4 Plant Biology. San Diego, USA: Academic Press, Mallmann J, Heckmann D, Bräutigam A, Lercher MJ, Weber AP, Westhoff P, Gowik U The role of photorespiration during the evolution of C 4 photosynthesis in the genus Flaveria. elife 3, e Mckown, A. D., Moncalvo, J. M. and Dengler N. G Phylogeny of Flaveria (Asteraceae) and inference of C 4 photosynthesis evolution. American Journal of Botany 92: McKown AD, Dengler NG Key innovations in the evolution of Kranz anatomy and C 4 vein pattern in Flaveria (Asteraceae). American Journal of Botany 94: Meister M, Agostino A, Hatch MD The roles of malate and aspartate in C 4 photosynthetic metabolism of Flaveria bidentis (L.) Planta 199: Monson RK, Teeri JA, Ku MS, Gurevitch J, Mets LJ, Dudley S Carbon-isotope discrimination by leaves of Flaveria species exhibiting different amounts of C 3 -and C 4 -cycle co-function. Planta 174: Monson RK, Moore Bd, Ku MSB, Edward GE Co-function of C 3 - and C 4 -photosynthetic pathways in C 3, C 4 and C 3 -C 4 intermediate Flaveria species. Planta 168: Moore BD and Edwards GE Photosynthetic induction in a C 4 dicot, Flaveria trinervia Plant Physiol. 81: Moore Bd, Ku MSB, Edwards GE Expression of C 4 -like photosynthesis in several species of Flaveria. Plant, Cell & Environment 12: Moore Bd, Monson RK, Ku MSB, Edwards GE Activities of principal photosynthetic and photorespiratory enzymes in leaf mesophyll and bundle sheath protoplasts from the C 3 -C 4 intermediate Flaveriaramosissima. Plant Cell Physiology 29: Nakamura, N., Iwano, M., Havaux, M., Yokota, A., Munekage, Y.N Promotion of cyclic electron transport around photosystem I during the evolution of NADP-malic enzyme-type C 4 photosynthesis in the genus Flaveria. New Phytologist. 199: Patel M and Berry JO Rubisco gene expression in C 4 plants. J Exp Bot. 59: Patel M, Siegel AJ, Berry JO Untranslated regions of FbRbcS1 mrna mediate bundle sheath cell-specific gene expression in leaves of a C 4 plant. J Biol Chem. 281: Y. N. Munekage & Y. Y. Taniguchi-7

8 Powell, A. M Systematics of Flaveria (Flaveriinae Asteraceae). Annals of the Missouri Botanical Garden 65: Sage, T.L., Busch, F.A., Johnson, D.C., Friesen, P.C., Stinson, C.R., Stata, M., Sultmanis, S., Rahman, B.A., Rawsthorne, S., & Sage, R.F Initial events during the evolution of C 4 photosynthesis in C 3 species of Flaveria. Plant Physiol, 163: Sage RF, Christin PA, Edward EJ The C 4 plant lineages of planet Earth. Journal of Experimental Botany 62: Sage RF, Khoshravesh R and Sage TL From proto-kranz to C 4 Kranz: building the bridge to C 4 photosynthesis J Exp Bot. 65: Sage RF, Sage TL, Kocacinar K Photorespiration and the evolution of C 4 photosynthesis. Annual Review of Plant Biology 63: Schulze S, Mallmann J, Burscheidt J, Koczor M, Streubel M, Bauwe H, Gowik U, Westhoff P Evolution of C 4 photosynthesis in the genus Flaveria: establishment of a photorespiratory CO 2 pump. Plant Cell. 25: Y. N. Munekage & Y. Y. Taniguchi-8