Regulation of Ethylene Biosynthesis at the Level of 1-Aminocyclopropane-1-Carboxylate

Regulation of ethylene biosynthesis at the level of 1-aminocyclopropane-1-carboxylate oxidase (ACO) gene

Izabela Ruduś1, Magdalena Sasiak2, Jan Kępczyński1 ()

1Department of Plant Physiology and Genetic Engineering, Szczecin University, ul. Wąska 13, 71-415 Szczecin, Poland 2Medical Diagnostic Laboratory, The Regional Specialist Hospital,ul. Hubalczyków 1, 76-200 Słupsk, Poland

Author for correspondence: Tel: +48 91 4441544 Fax: +48 91 4441589 Email: [email protected]

Table S1 ACO gene families identified in different seed plant species.

Organism ACO gene symbol GenBank Type of nucleic acid U References accession n number i P r o t a c c e s s i o n n u m b e r ACTINIDIACEAE Actinidia deliciosa AD-ACO1 M97961 mRNA P MacDiarmid and Gardner (1993) 3 1 2 3 7 AD-ACO2 HQ293205 mRNA G Atkinson et al. (2011) 3 D S B 7 AD-ACO3 HQ293207 mRNA G Atkinson et al. (2011) 3 D S B 9 AD-ACO4 HQ293209 mRNA G Atkinson et al. (2011) 3 D S C 1 AD-ACO5 HQ293211 mRNA G Atkinson et al. (2011) 3 D S C 3 ASTERACEAE Helianthus annuus HA-ACO1 U62553 DNA Q Liu et al. (1997) 7 D M E 6 L29405 mRNA Q Liu et al. (1997) 3 9 9 3 3 HA-ACO2 U62554 mRNA partial cds Q Liu et al. (1997) 3 9 9 6 0 HA-ACO3 U62555 mRNA partial cds Q Liu et al. (1997) 3 9 9 6 1 X92651 mRNA partial cds Q Ouvrard et al. (1996) 3 9 9 3 4 Lactuca sativa LS-ACO1 AB158345 mRNA B Takahashi et al. (2010) 9 A 0 T 8 LS-ACO2 AB158346 mRNA B Takahashi et al. (2010) 9 A 0 T 9 LS-ACO3 AB158347 mRNA B Takahashi et al. (2010) 9 A 0 U 0 BETULACEAE Betula pendula BP-ACO1 X97993 mRNA partial cds Q Tuomainen [GB] 7 D L W 6 Y10749 mRNA Q Järveläinen et al. (1997); Vahala et al. (2003) 3 9 3 9 6 BP-ACO2 AY154649 mRNA Q Vahala et al. (2003) 7 Y 2 5 7 BP-ACO3 X97992 mRNA partial cds Q Tuomainen [GB] 3 9 3 9 7 BP-ACO5 X97994 mRNA partial cds Q Tuomainen [GB] 3 9 3 9 8 BRASSICACEAE Arabidopsis thaliana AT-ACO1 (At2g19590) NM_127517 mRNA Q Lin et al. (1999); Garcia et al. (2010) 9 Z U N 4 AF370195 mRNA Q Yamada et al. [GB] 9 Z U N 4 AY062951 mRNA Q Yamada et al. [GB] 9 Z U N 4 AT-ACO2 (At1g62380) NM_104918 mRNA Q Theologis et al. (2000); Qin et al. (2007); 4 Garcia et al. (2010) 1 9 3 1 AF016100 mRNA Q Ecker and Raz [GB] 4 1 9 3 1 AY133851 mRNA Q Yamada et al. [GB] 4 1 9 3 1 AY045876 mRNA Q Yamada et al. [GB] 4 1 9 3 1 AT-ACO3 (At1g12010) NM_101073 mRNA O Theologis et al. (2000) 6 5 3 7 8 AT-ACO4 (At1g05010) NM_100380 mRNA Q Gómez-Lim et al. (1993); Theologis et al. 0 (2000); Qin et al. (2007) 6 5 8 8 AT-ACO5 (At1g77330) NM_106382 mRNA Q Theologis et al. (2000) 0 W P W 4 AT-ACOH4 (At1g03400) NM_100222 mRNA Q Theologis et al. (2000) 9 4 A 7 8 AT-ACOH8 (At3G61400) NM_116004 mRNA Q Salanoubat et al. (2000) 9 M 2 C 4 AT-ACOH9 (At5g43440) NM_123710 mRNA Q Swarbreck et al. [GB] 9 L S W 7 AT-ACOH10(At5g43450) NM_123711 mRNA Q Swarbreck et al. [GB] 9 L S W 6 Fe2OG (At3G47190) NM_114586 mRNA F Salanoubat et al. (2000) 4 J A D 4 Fe2OG-like (At2G30830) NM_128636 mRNA O Lin et al. (1999) 8 0 8 5 0 Fe2OG-like (At2G30840) NM_128637 mRNA O Lin et al. (1999) 8 0 8 5 1 putative 2OA DIOX NM_128102 mRNA Q Lin et al. (1999) (At2g25450) 9 S K K 4 Brassica oleracea BO-ACO1 X81628 mRNA Q Pogson et al. (1995) 4 3 4 0 4 BO-ACO2 X81629 mRNA Q Pogson et al. (1995) 4 3 4 0 5 BO-ACO3 AF252853 mRNA Q Yang et al. (2003) 8 G T A 4 Brassica rapa BR-ACO1 AJ309321 mRNA Q Rodríguez-Gacio et al. (2004) 9 4 I N 6 BR-ACO2 AJ309322 mRNA Q Rodríguez-Gacio et al. (2004) 7 F N W 0 Lepidium sativum LS-ACO1 GQ221031 mRNA partial C Linkies et al. (2009) 7 D T J 9 LS-ACO2 GQ221032 mRNA C Linkies et al. (2009) 7 D T K 0 LS-ACO4 GQ221033 mRNA partial C Linkies et al. (2009) 7 D T K 1 CARICACEAE Carica papaya CP-ACO1 L76283 mRNA Q Chi- Tsai and Ming- Tse [GB] 3 9 5 4 9 AJ851006 mRNA partial Q Lam et al. [GB] 5 W M 3 2 AJ852507 mRNA Q Abubakar and Lam [GB] 5 W 1 K 1 AY077461 mRNA Q Varona et al. [GB] 8 S 9 H 5 ACO2 (CP-ACO1)a AY455668 mRNA Q Burns and Kumdee [GB] 3 3 0 J 7 AY601705 DNA Q Burns et al. [GB] 5 3 A S 3 CP-ACO2 U68215 mRNA Q Neupane et al. [GB] 9 Z R C 9 AF254125 mRNA Q Zainal et al. [GB] 9 M 4 U 2 AF320071 mRNA Q Chen et al. (2003b) 8 W 2 D 6 AF379855 DNA Q López-Gómez et al. (2004) 9 4 J L 7 AJ507013 mRNA partial Q Saiprasad [GB] 7 0 X T 0 AJ605321 mRNA Q Saiprasad and Lalitha [GB] 9 Z R C 9 AJ851239 mRNA Q Sew et al. [GB] 5 W 1 M 7 AJ853461 mRNA Q Sew et al. [GB] 9 Z R C 9 ACO1 (CP-ACO2)a AY455667 mRNA Q Burns and Kumdee [GB] 9 4 J L 7 AY601704 DNA Q Burns et al. [GB] 9 4 J L 7 CUCURBITACEAE Cucumis melo CM-ACO1 X95551 DNA Q Lasserre et al. (1996) 0 4 6 4 4 AB522604 DNA C Huang et al. (2010) 8 K I S 1 D31727 mRNA Q Yamamoto et al. [GB] 0 4 6 4 4 GU017416 mRNA D Hao et al. [GB] 0 V 4 H 6 CM-ACO2 X95552 DNA Q Lasserre et al. (1996) 4 3 4 1 9 CM-ACO3 X95553 DNA P Lasserre et al. (1996) 5 4 8 4 7 Cucumis sativus CS-ACO1 AF033581 mRNA O Perl-Treves et al. (1998); Kahana et al. (1999) 6 4 9 4 5 FN544066 mRNA C Bhardway et al. [GB] 7 U 1 K 1 CS-ACO2 AF033582 mRNA partial O Perl-Treves et al. (1998); Kahana et al. (1999) 6 4 9 4 6 CS-ACO3 AF033583 mRNA O Perl-Treves et al. (1998); Kahana et al. (1999) 6 4 9 4 7 AY450356 DNA Q Chen et al. [GB] 6 J J 1 0 CS-ACO1 (CS-ACO3)b AB006806 mRNA O Shiomi et al. (1998) 8 2 1 2 6 CS-ACO2 (CS-ACO1)b AB006807 mRNA O Shiomi et al. (1998) 8 2 1 2 7 EBENACEAE Diospyros kaki DK-ACO1 AB073008 mRNA Q Nakano et al. (2003) 8 S 9 3 2 DK-ACO2 AB073009 mRNA Q Nakano et al. (2003) 8 S 9 3 1 EUPHORBIACEAE Hevea brasiliensis HB-ACO1 AM743170 mRNA A Hadi [GB] 5 I 8 L 4 AM743173 mRNA ex.1-4 A Hadi [GB] 5 I 8 L 7 HB-ACO2 AM743171 mRNA Q Hadi [GB] 5 V L J 5 AM743174 mRNA ex.1-3 A Hadi [GB] 5 I 8 L 8 AY207387 mRNA Q Kongsawadworakul and Chrestin [GB] 5 V L J 5 HB-ACO3 AM743172 mRNA A Hadi [GB] 5 I 8 L 6 Manihot esculenta ME-ACO1 EF035079 mRNA A Beeching and Han [GB] 0 S V L 8 ME-ACO2 AY973618 mRNA Q Reilly et al. (2007) 5 2 Q X 6 ME-ACO3 EF055260 DNA A Beeching and Li [GB] 0 S W U 5 FABACEAE Trifolium repens TR-ACO1 DQ112347 DNA Q Chen and McManus (2006) 9 X E R 2 AF115261 mRNA Q Hunter et al. (1999) 9 X E R 2 TR-ACO2 DQ112348 DNA Q Chen and McManus (2006) 9 X E R 3 AF115262 mRNA Q Hunter et al. (1999) 9 X E R 3 TR-ACO3 DQ112349 DNA Q Chen and McManus (2006) 2 V J 1 4 AF115263 mRNA Q Hunter et al. (1999) 9 X E R 4 TR-ACO4 DQl12350 DNA Q Chen and McManus (2006) 2 V J 1 3 Vicia faba VF-ACO1 EU543653 mRNA partial D Zhou et al. (2010) 2 C P U 6 VF-ACO2 EU543654 mRNA partial D Zhou et al. (2010) 2 C P U 7 Vigna radiata VR-ACO1 AM180696 DNA Q Dieu et al. [GB] 2 K T E 6 VR-ACO2 AM180697 DNA Q Dieu et al. [GB] 2 K T E 5 VR-ACO3 AM180698 DNA Q Dieu et al. [GB] 2 K T E 4 VR-ACO4 AM180699 DNA Q Dieu et al. [GB] 2 K T E 3 VR-ACO AF315316 DNA Q Park et al. [GB] 7 F Y 6 2 VR-ACO homolog U06046 mRNA Q Kim and Yang [GB]; Kim [GB} 4 1 6 8 1 GERANIACEAE Pelargonium hortorum PH-ACO1 U07953 mRNA Q Wang et al. (1994) 4 3 6 1 3 PH-ACO2 U19856 mRNA Q Clark et al. (1997) 4 0 8 7 6 PH-ACO3 U67861 mRNA O Clark et al. (1997) 2 4 2 6 5 LILIACEAE Tulipa gesneriana TG-ACO1 AB232765 mRNA Q Momonoi et al. (2007) 4 0 0 V 0 TG-ACO2 AB232766 mRNA Q Momonoi et al. (2007) 4 0 0 U 9 TG-ACO3 AB232767 mRNA Q Momonoi et al. (2007) 4 0 0 P 0 TG-ACO4 AB232768 mRNA Q Momonoi et al. (2007) 4 0 0 U 7 TG-ACO AB161946 mRNA Q Momonoi et al. (2007) 7 5 Q N 1 LINACEAE Linum usitatissimum LU-ACO1 EF661825 mRNA partial A Zhao and Hasenstein (2009) 6 Z I 3 0 LU-ACO2 EF661826 mRNA partial A Zhao and Hasenstein (2009) 6 Z I 3 1 LU-ACO3 EF661827 mRNA partial A Zhao and Hasenstein (2009) 6 Z I 3 2 MALVACEAE Gossypium hirsutum GH-ACO1 DQ116442 mRNA Q Shi et al. (2006) 2 Q D G 0 DQ303122 mRNA Q Hu et al. [GB] 2 P T 7 4 GH-ACO2 DQI16443 mRNA Q Shi et al. (2006) 2 Q D F 9 GH-ACO3 DQI16444 mRNA Q Shi et al. (2006) 2 Q D F 8 GH-ACO4 DQ122175 mRNA Q Shi et al. (2006) 2 Q C Y 1 PINACEAE Pinus taeda PT-ACO1 GQ258776 DNA D Yuan et al (2010) 4 N 2 S 4 PT-ACO2 GQ258775 DNA D Yuan et al (2010) 4 N 2 S 3 PT-ACO3 GQ258774 DNA D Yuan et al (2010) 4 N 2 S 2 PT-ACO4 GQ258773 DNA Yuan et al (2010) PT-ACO5 GQ258772 DNA Yuan et al (2010) PLANTAGINACEAE Antirrhinum majus AM-ACO1 AY333925 mRNA partial Q Woltering and Nijenhuis de Vries [GB] 7 X B E 6 AM-ACO2 AY333926 mRNA partial Q Woltering and Nijenhuis de Vries [GB] 7 X B E 5 POACEAE Oryza sativa OS-ACO1 X85747 mRNA A Mekhedov and Kende (1996) 2 Z 1 W 9 OS-ACO2 AF049888 mRNA partial O Chae et al. (2000) 6 5 0 3 0 OS-ACO3 AF049889 mRNA O Chae et al. (2000) 6 5 0 3 1 Sorghum bicolor SB-ACO1 AF079588 mRNA O Finlayson et al. (1999) 8 1 6 0 6 SB-ACO2 AF079589 mRNA partial O Finlayson et al. (1999) 8 1 6 0 7 Zea mays ZM-ACO1 AY155581 mRNA partial Q Siriwitayawan et al. [GB] 2 T V K 1 ZM-ACO15 AY359572 DNA Q Gallie and Young (2004) 6 J N 5 6 ZM-ACO20 AY359574 DNA Q Gallie and Young (2004) 3 Z T U 5 AY359575 mRNA Q Gallie and Young (2004) 6 J N 5 4 ZM-ACO31 AY359573 mRNA Q Gallie and Young (2004) 6 J N 5 5 ZM-ACO35 AY359576 DNA Q Gallie and Young (2004) 6 J N 5 3 POLYGONACEAE Rumex palustris RP-ACO1 Y10034 mRNA P Vriezen et al. (1999) 9 3 4 5 9 RP-ACO2 AF041479 mRNA O Vriezen et al. (1999) 4 9 1 7 0 RHAMNACEAE Ziziphus jujuba ZJ-ACO1 EU216549 mRNA A Wei et al. [GB] 8 W B X 5 JF812966 mRNA G Chen and Chen [GB] 4 X H S 7 ZJ-ACO2 EU216550 mRNA A Wei et al. [GB] 8 W B X 6 ROSACEAE Malus domestica MD-ACO1 X98627 DNA P Castiglione et al. [GB] 9 3 2 6 9 Y14005 DNA Q Castiglione et al. [GB] 0 0 9 8 5 AF030859 DNA Q Atkinson et al. (1998) 0 0 9 8 5 AY598766 DNA partial Q Costa et al. (2005) 6 P L 0 1 AY598767 DNA partial Q Costa et al. (2005) 6 P L 0 2 AY598768 DNA partial Q Costa et al. (2005) 6 P L 0 1 DQ137848 mRNA Q Li et al. [GB] 0 R 3 6 8 DQ137850 mRNA Q Li et al. [GB] 0 R 3 6 6 AJ001646 mRNA P Castiglione et al. [GB] 9 3 2 6 9 MD-ACO2 AF015787 DNA O Nam and Kim [GB] 4 8 8 8 2 DQ438990 mRNA partial C Dal Cin et al. (2007) 5 E 7 H 2 MD-ACO3 AB086888 mRNA Q Hatsuyama et al. [GB] 8 H 0 C 8 Prunus persica PP-ACO1 AF129073 DNA Q Ruperti et al (2001) 4 3 6 1 8 AF532976 DNA Q Moon and Callahan (2004) 4 3 6 1 8 AF319166 mRNA Q Callahan et al. (1992 ) 4 3 6 1 8 X77232 mRNA Q Lester et al. (1994) 4 3 6 1 8 AB044711 mRNA partial cds Q Mathooko et al. (2004) 9 L R C 0 PP-ACO2 AB044712 mRNA partial cds Q Mathooko et al. (2004) 9 L R B 9 AF129074 DNA Q Ruperti et al (2001) 9 M 7 K 5 SALICACEAE Populus trichocarpa ACO1 XM_002300926 mRNA B Tuskan et al (2006) 9 G T Z 8 ACO2 XM_002302820 mRNA A Tuskan et al (2006) 9 P H S 1 ACO3 XM_002320451 mRNA A Tuskan et al (2006) 9 P I 6 6 ACO4 XM_002307425 mRNA B Tuskan et al (2006) 9 H 7 J 4 ACO5 XM_002309191 mRNA B Tuskan et al (2006) 9 H 8 X 0 ACO6 XM_002331492 mRNA B Tuskan et al (2006) 9 N 8 H 1 ACO7 XM_002316553 mRNA B Tuskan et al (2006) 9 H Z H 4 SOLANACEAE Lycopersicon esculentum LE-ACO1 X58273 DNA P Köck et al. (1991) 0 5 1 1 6 X04792 mRNA P Holdsworth et al. (1987b) 0 5 1 1 6 NM_001247095 mRNA P Köck et al. (1991); Holdsworth et al. (1987b) 0 5 1 1 6 HQ322499 mRNA E Jafari et al. [GB] 3 V W N 6 LE-ACO2 Y00478 DNA P Holdsworth et al. (1987a) 0 7 9 2 0 LE-ACO3 Z54199 DNA P Barry et al. (1996) 2 4 1 5 7 NM_001246999 mRNA P Blume et al. (1997); Barry et al. (1996) 2 4 1 5 7 LE-ACO4 AB013101 mRNA Q Nakatsuka et al. (1998) 9 Z W P 2 NM_001246938 mRNA Q Nakatsuka et al. (1998) 9 Z W P 2 LE-ACO5 AJ715790 mRNA Q Sell and Hehl (2005) 6 A 1 K 7 NM_001247108 mRNA Q Sell and Hehl (2005) 6 A 1 K 7 Nicotiana attenuata NA-ACO1 AY426756 mRNA Q Winz et al. [GB]; Lou and Baldwin (2004) 6 H 2 3 7 NA-ACO2a EF123109 mRNA partial A Winz et al. [GB]; Barazani et al. (2007) 7 K A V 3 NA-ACO2b EF123110 mRNA partial B Winz et al. [GB] 7 S 4 X 2 NA-ACO3 EF123111 mRNA A Winz et al. [GB]; Barazani et al. (2007) 7 K A V 4 Nicotiana glutinosa NG-ACO1 U54565 mRNA O Kim et al. (1998) 2 4 1 0 8 NG-ACO2 U54566 mRNA O Kim et al. (1998) 2 4 1 0 9 NG-ACO3 U62764 mRNA Q Kim et al. (1998) 4 0 3 9 9 Petunia hybrida PH-ACO1 L21976 DNA Q Tang et al. (1993) 0 8 5 0 6 PH-ACO2 L21977 DNA Tang et al. (1993) PH-ACO3 L21978 DNA Q Tang et al. (1993) 0 8 5 0 7 PH-ACO4 L21979 DNA Q Tang et al. (1993) 0 8 5 0 8 Solanum tuberosum ST-ACO1 AF384820 mRNA Q Nie et al. (2002) 9 4 F 6 6 ST-ACO2 AF384821 mRNA Q Nie et al. (2002) 9 4 F 6 5 ST-ACO3 AY098939 mRNA Q Zanetti et al. (2002) 8 G V B 6 The nomenclature of the presented gene families has been unified, so that the three letter symbol ACO (ACC oxidase) is preceeded by the Latin initials of each species. The genes are italicized and in most cases numbered chronologically according to deposition of the sequence in GenBank [GB]. a,b the homology analysis of nucleotide and amino acid sequences indicated that the paralogs of ACO gene in C. papaya and C. sativus should be re-numbered

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