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:

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

Organism / ACO gene symbol / GenBank accession number / Type of nucleic acid / UniProt accession number / References
ACTINIDIACEAE
Actinidia deliciosa / AD-ACO1 / M97961 / mRNA / P31237 / MacDiarmid and Gardner (1993)
AD-ACO2 / HQ293205 / mRNA / G3DSB7 / Atkinson et al. (2011)
AD-ACO3 / HQ293207 / mRNA / G3DSB9 / Atkinson et al. (2011)
AD-ACO4 / HQ293209 / mRNA / G3DSC1 / Atkinson et al. (2011)
AD-ACO5 / HQ293211 / mRNA / G3DSC3 / Atkinson et al. (2011)
ASTERACEAE
Helianthus annuus / HA-ACO1 / U62553 / DNA / Q7DME6 / Liu et al. (1997)
L29405 / mRNA / Q39933 / Liu et al. (1997)
HA-ACO2 / U62554 / mRNA partial cds / Q39960 / Liu et al. (1997)
HA-ACO3 / U62555 / mRNA partial cds / Q39961 / Liu et al. (1997)
X92651 / mRNA partial cds / Q39934 / Ouvrard et al. (1996)
Lactuca sativa / LS-ACO1 / AB158345 / mRNA / B9A0T8 / Takahashi et al. (2010)
LS-ACO2 / AB158346 / mRNA / B9A0T9 / Takahashi et al. (2010)
LS-ACO3 / AB158347 / mRNA / B9A0U0 / Takahashi et al. (2010)
BETULACEAE
Betula pendula / BP-ACO1 / X97993 / mRNA partial cds / Q7DLW6 / Tuomainen [GB]
Y10749 / mRNA / Q39396 / Järveläinen et al. (1997); Vahala et al. (2003)
BP-ACO2 / AY154649 / mRNA / Q7Y257 / Vahala et al. (2003)
BP-ACO3 / X97992 / mRNA partial cds / Q39397 / Tuomainen [GB]
BP-ACO5 / X97994 / mRNA partial cds / Q39398 / Tuomainen [GB]
BRASSICACEAE
Arabidopsis thaliana / AT-ACO1 (At2g19590) / NM_127517 / mRNA / Q9ZUN4 / Lin et al. (1999); Garcia et al. (2010)
AF370195 / mRNA / Q9ZUN4 / Yamada et al. [GB]
AY062951 / mRNA / Q9ZUN4 / Yamada et al. [GB]
AT-ACO2 (At1g62380) / NM_104918 / mRNA / Q41931 / Theologis et al. (2000); Qin et al. (2007); Garcia et al. (2010)
AF016100 / mRNA / Q41931 / Ecker and Raz [GB]
AY133851 / mRNA / Q41931 / Yamada et al. [GB]
AY045876 / mRNA / Q41931 / Yamada et al. [GB]
AT-ACO3 (At1g12010) / NM_101073 / mRNA / O65378 / Theologis et al. (2000)
AT-ACO4 (At1g05010) / NM_100380 / mRNA / Q06588 / Gómez-Lim et al. (1993); Theologis et al. (2000); Qin et al. (2007)
AT-ACO5 (At1g77330) / NM_106382 / mRNA / Q0WPW4 / Theologis et al. (2000)
AT-ACOH4 (At1g03400) / NM_100222 / mRNA / Q94A78 / Theologis et al. (2000)
AT-ACOH8 (At3G61400) / NM_116004 / mRNA / Q9M2C4 / Salanoubat et al. (2000)
AT-ACOH9 (At5g43440) / NM_123710 / mRNA / Q9LSW7 / Swarbreck et al. [GB]
AT-ACOH10(At5g43450) / NM_123711 / mRNA / Q9LSW6 / Swarbreck et al. [GB]
Fe2OG (At3G47190) / NM_114586 / mRNA / F4JAD4 / Salanoubat et al. (2000)
Fe2OG-like (At2G30830) / NM_128636 / mRNA / O80850 / Lin et al. (1999)
Fe2OG-like (At2G30840) / NM_128637 / mRNA / O80851 / Lin et al. (1999)
putative 2OA DIOX (At2g25450) / NM_128102 / mRNA / Q9SKK4 / Lin et al. (1999)
Brassica oleracea / BO-ACO1 / X81628 / mRNA / Q43404 / Pogson et al. (1995)
BO-ACO2 / X81629 / mRNA / Q43405 / Pogson et al. (1995)
BO-ACO3 / AF252853 / mRNA / Q8GTA4 / Yang et al. (2003)
Brassica rapa / BR-ACO1 / AJ309321 / mRNA / Q94IN6 / Rodríguez-Gacio et al. (2004)
BR-ACO2 / AJ309322 / mRNA / Q7FNW0 / Rodríguez-Gacio et al. (2004)
Lepidium sativum / LS-ACO1 / GQ221031 / mRNA partial / C7DTJ9 / Linkies et al. (2009)
LS-ACO2 / GQ221032 / mRNA / C7DTK0 / Linkies et al. (2009)
LS-ACO4 / GQ221033 / mRNA partial / C7DTK1 / Linkies et al. (2009)
CARICACEAE
Carica papaya / CP-ACO1 / L76283 / mRNA / Q39549 / Chi- Tsai and Ming- Tse [GB]
AJ851006 / mRNA partial / Q5WM32 / Lam et al. [GB]
AJ852507 / mRNA / Q5W1K1 / Abubakar and Lam [GB]
AY077461 / mRNA / Q8S9H5 / Varona et al. [GB]
ACO2 (CP-ACO1)a / AY455668 / mRNA / Q330J7 / Burns and Kumdee [GB]
AY601705 / DNA / Q53AS3 / Burns et al. [GB]
CP-ACO2 / U68215 / mRNA / Q9ZRC9 / Neupane et al. [GB]
AF254125 / mRNA / Q9M4U2 / Zainal et al. [GB]
AF320071 / mRNA / Q8W2D6 / Chen et al. (2003b)
AF379855 / DNA / Q94JL7 / López-Gómez et al. (2004)
AJ507013 / mRNA partial / Q70XT0 / Saiprasad [GB]
AJ605321 / mRNA / Q9ZRC9 / Saiprasad and Lalitha [GB]
AJ851239 / mRNA / Q5W1M7 / Sew et al. [GB]
AJ853461 / mRNA / Q9ZRC9 / Sew et al. [GB]
ACO1 (CP-ACO2)a / AY455667 / mRNA / Q94JL7 / Burns and Kumdee [GB]
AY601704 / DNA / Q94JL7 / Burns et al. [GB]
CUCURBITACEAE
Cucumis melo / CM-ACO1 / X95551 / DNA / Q04644 / Lasserre et al. (1996)
AB522604 / DNA / C8KIS1 / Huang et al. (2010)
D31727 / mRNA / Q04644 / Yamamoto et al. [GB]
GU017416 / mRNA / D0V4H6 / Hao et al. [GB]
CM-ACO2 / X95552 / DNA / Q43419 / Lasserre et al. (1996)
CM-ACO3 / X95553 / DNA / P54847 / Lasserre et al. (1996)
Cucumis sativus / CS-ACO1 / AF033581 / mRNA / O64945 / Perl-Treves et al. (1998); Kahana et al. (1999)
FN544066 / mRNA / C7U1K1 / Bhardway et al. [GB]
CS-ACO2 / AF033582 / mRNA partial / O64946 / Perl-Treves et al. (1998); Kahana et al. (1999)
CS-ACO3 / AF033583 / mRNA / O64947 / Perl-Treves et al. (1998); Kahana et al. (1999)
AY450356 / DNA / Q6JJ10 / Chen et al. [GB]
CS-ACO1 (CS-ACO3)b / AB006806 / mRNA / O82126 / Shiomi et al. (1998)
CS-ACO2 (CS-ACO1)b / AB006807 / mRNA / O82127 / Shiomi et al. (1998)
EBENACEAE
Diospyros kaki / DK-ACO1 / AB073008 / mRNA / Q8S932 / Nakano et al. (2003)
DK-ACO2 / AB073009 / mRNA / Q8S931 / Nakano et al. (2003)
EUPHORBIACEAE
Hevea brasiliensis / HB-ACO1 / AM743170 / mRNA / A5I8L4 / Hadi [GB]
AM743173 / mRNA ex.1-4 / A5I8L7 / Hadi [GB]
HB-ACO2 / AM743171 / mRNA / Q5VLJ5 / Hadi [GB]
AM743174 / mRNA ex.1-3 / A5I8L8 / Hadi [GB]
AY207387 / mRNA / Q5VLJ5 / Kongsawadworakul and Chrestin [GB]
HB-ACO3 / AM743172 / mRNA / A5I8L6 / Hadi [GB]
Manihot esculenta / ME-ACO1 / EF035079 / mRNA / A0SVL8 / Beeching and Han [GB]
ME-ACO2 / AY973618 / mRNA / Q52QX6 / Reilly et al. (2007)
ME-ACO3 / EF055260 / DNA / A0SWU5 / Beeching and Li [GB]
FABACEAE
Trifolium repens / TR-ACO1 / DQ112347 / DNA / Q9XER2 / Chen and McManus (2006)
AF115261 / mRNA / Q9XER2 / Hunter et al. (1999)
TR-ACO2 / DQ112348 / DNA / Q9XER3 / Chen and McManus (2006)
AF115262 / mRNA / Q9XER3 / Hunter et al. (1999)
TR-ACO3 / DQ112349 / DNA / Q2VJ14 / Chen and McManus (2006)
AF115263 / mRNA / Q9XER4 / Hunter et al. (1999)
TR-ACO4 / DQl12350 / DNA / Q2VJ13 / Chen and McManus (2006)
Vicia faba / VF-ACO1 / EU543653 / mRNA partial / D2CPU6 / Zhou et al. (2010)
VF-ACO2 / EU543654 / mRNA partial / D2CPU7 / Zhou et al. (2010)
Vigna radiata / VR-ACO1 / AM180696 / DNA / Q2KTE6 / Dieu et al. [GB]
VR-ACO2 / AM180697 / DNA / Q2KTE5 / Dieu et al. [GB]
VR-ACO3 / AM180698 / DNA / Q2KTE4 / Dieu et al. [GB]
VR-ACO4 / AM180699 / DNA / Q2KTE3 / Dieu et al. [GB]
VR-ACO / AF315316 / DNA / Q7FY62 / Park et al. [GB]
VR-ACO homolog / U06046 / mRNA / Q41681 / Kim and Yang [GB]; Kim [GB}
GERANIACEAE
Pelargonium hortorum / PH-ACO1 / U07953 / mRNA / Q43613 / Wang et al. (1994)
PH-ACO2 / U19856 / mRNA / Q40876 / Clark et al. (1997)
PH-ACO3 / U67861 / mRNA / O24265 / Clark et al. (1997)
LILIACEAE
Tulipa gesneriana / TG-ACO1 / AB232765 / mRNA / Q400V0 / Momonoi et al. (2007)
TG-ACO2 / AB232766 / mRNA / Q400U9 / Momonoi et al. (2007)
TG-ACO3 / AB232767 / mRNA / Q400P0 / Momonoi et al. (2007)
TG-ACO4 / AB232768 / mRNA / Q400U7 / Momonoi et al. (2007)
TG-ACO / AB161946 / mRNA / Q75QN1 / Momonoi et al. (2007)
LINACEAE
Linum usitatissimum / LU-ACO1 / EF661825 / mRNA partial / A6ZI30 / Zhao and Hasenstein (2009)
LU-ACO2 / EF661826 / mRNA partial / A6ZI31 / Zhao and Hasenstein (2009)
LU-ACO3 / EF661827 / mRNA partial / A6ZI32 / Zhao and Hasenstein (2009)
MALVACEAE
Gossypium hirsutum / GH-ACO1 / DQ116442 / mRNA / Q2QDG0 / Shi et al. (2006)
DQ303122 / mRNA / Q2PT74 / Hu et al. [GB]
GH-ACO2 / DQI16443 / mRNA / Q2QDF9 / Shi et al. (2006)
GH-ACO3 / DQI16444 / mRNA / Q2QDF8 / Shi et al. (2006)
GH-ACO4 / DQ122175 / mRNA / Q2QCY1 / Shi et al. (2006)
PINACEAE
Pinus taeda / PT-ACO1 / GQ258776 / DNA / D4N2S4 / Yuan et al (2010)
PT-ACO2 / GQ258775 / DNA / D4N2S3 / Yuan et al (2010)
PT-ACO3 / GQ258774 / DNA / D4N2S2 / Yuan et al (2010)
PT-ACO4 / GQ258773 / DNA / Yuan et al (2010)
PT-ACO5 / GQ258772 / DNA / Yuan et al (2010)
PLANTAGINACEAE
Antirrhinum majus / AM-ACO1 / AY333925 / mRNA partial / Q7XBE6 / Woltering and Nijenhuis de Vries [GB]
AM-ACO2 / AY333926 / mRNA partial / Q7XBE5 / Woltering and Nijenhuis de Vries [GB]
POACEAE
Oryza sativa / OS-ACO1 / X85747 / mRNA / A2Z1W9 / Mekhedov and Kende (1996)
OS-ACO2 / AF049888 / mRNA partial / O65030 / Chae et al. (2000)
OS-ACO3 / AF049889 / mRNA / O65031 / Chae et al. (2000)
Sorghum bicolor / SB-ACO1 / AF079588 / mRNA / O81606 / Finlayson et al. (1999)
SB-ACO2 / AF079589 / mRNA partial / O81607 / Finlayson et al. (1999)
Zea mays / ZM-ACO1 / AY155581 / mRNA partial / Q2TVK1 / Siriwitayawan et al. [GB]
ZM-ACO15 / AY359572 / DNA / Q6JN56 / Gallie and Young (2004)
ZM-ACO20 / AY359574 / DNA / Q3ZTU5 / Gallie and Young (2004)
AY359575 / mRNA / Q6JN54 / Gallie and Young (2004)
ZM-ACO31 / AY359573 / mRNA / Q6JN55 / Gallie and Young (2004)
ZM-ACO35 / AY359576 / DNA / Q6JN53 / Gallie and Young (2004)
POLYGONACEAE
Rumex palustris / RP-ACO1 / Y10034 / mRNA / P93459 / Vriezen et al. (1999)
RP-ACO2 / AF041479 / mRNA / O49170 / Vriezen et al. (1999)
RHAMNACEAE
Ziziphus jujuba / ZJ-ACO1 / EU216549 / mRNA / A8WBX5 / Wei et al. [GB]
JF812966 / mRNA / G4XHS7 / Chen and Chen [GB]
ZJ-ACO2 / EU216550 / mRNA / A8WBX6 / Wei et al. [GB]
ROSACEAE
Malus domestica / MD-ACO1 / X98627 / DNA / P93269 / Castiglione et al. [GB]
Y14005 / DNA / Q00985 / Castiglione et al. [GB]
AF030859 / DNA / Q00985 / Atkinson et al. (1998)
AY598766 / DNA partial / Q6PL01 / Costa et al. (2005)
AY598767 / DNA partial / Q6PL02 / Costa et al. (2005)
AY598768 / DNA partial / Q6PL01 / Costa et al. (2005)
DQ137848 / mRNA / Q0R368 / Li et al. [GB]
DQ137850 / mRNA / Q0R366 / Li et al. [GB]
AJ001646 / mRNA / P93269 / Castiglione et al. [GB]
MD-ACO2 / AF015787 / DNA / O48882 / Nam and Kim [GB]
DQ438990 / mRNA partial / C5E7H2 / Dal Cin et al. (2007)
MD-ACO3 / AB086888 / mRNA / Q8H0C8 / Hatsuyama et al. [GB]
Prunus persica / PP-ACO1 / AF129073 / DNA / Q43618 / Ruperti et al (2001)
AF532976 / DNA / Q43618 / Moon and Callahan (2004)
AF319166 / mRNA / Q43618 / Callahan et al. (1992 )
X77232 / mRNA / Q43618 / Lester et al. (1994)
AB044711 / mRNA partial cds / Q9LRC0 / Mathooko et al. (2004)
PP-ACO2 / AB044712 / mRNA partial cds / Q9LRB9 / Mathooko et al. (2004)
AF129074 / DNA / Q9M7K5 / Ruperti et al (2001)
SALICACEAE
Populus trichocarpa / ACO1 / XM_002300926 / mRNA / B9GTZ8 / Tuskan et al (2006)
ACO2 / XM_002302820 / mRNA / A9PHS1 / Tuskan et al (2006)
ACO3 / XM_002320451 / mRNA / A9PI66 / Tuskan et al (2006)
ACO4 / XM_002307425 / mRNA / B9H7J4 / Tuskan et al (2006)
ACO5 / XM_002309191 / mRNA / B9H8X0 / Tuskan et al (2006)
ACO6 / XM_002331492 / mRNA / B9N8H1 / Tuskan et al (2006)
ACO7 / XM_002316553 / mRNA / B9HZH4 / Tuskan et al (2006)
SOLANACEAE
Lycopersicon esculentum / LE-ACO1 / X58273 / DNA / P05116 / Köck et al. (1991)
X04792 / mRNA / P05116 / Holdsworth et al. (1987b)
NM_001247095 / mRNA / P05116 / Köck et al. (1991); Holdsworth et al. (1987b)
HQ322499 / mRNA / E3VWN6 / Jafari et al. [GB]
LE-ACO2 / Y00478 / DNA / P07920 / Holdsworth et al. (1987a)
LE-ACO3 / Z54199 / DNA / P24157 / Barry et al. (1996)
NM_001246999 / mRNA / P24157 / Blume et al. (1997); Barry et al. (1996)
LE-ACO4 / AB013101 / mRNA / Q9ZWP2 / Nakatsuka et al. (1998)
NM_001246938 / mRNA / Q9ZWP2 / Nakatsuka et al. (1998)
LE-ACO5 / AJ715790 / mRNA / Q6A1K7 / Sell and Hehl (2005)
NM_001247108 / mRNA / Q6A1K7 / Sell and Hehl (2005)
Nicotiana attenuata / NA-ACO1 / AY426756 / mRNA / Q6H237 / Winz et al. [GB]; Lou and Baldwin (2004)
NA-ACO2a / EF123109 / mRNA partial / A7KAV3 / Winz et al. [GB]; Barazani et al. (2007)
NA-ACO2b / EF123110 / mRNA partial / B7S4X2 / Winz et al. [GB]
NA-ACO3 / EF123111 / mRNA / A7KAV4 / Winz et al. [GB]; Barazani et al. (2007)
Nicotiana glutinosa / NG-ACO1 / U54565 / mRNA / O24108 / Kim et al. (1998)
NG-ACO2 / U54566 / mRNA / O24109 / Kim et al. (1998)
NG-ACO3 / U62764 / mRNA / Q40399 / Kim et al. (1998)
Petunia hybrida / PH-ACO1 / L21976 / DNA / Q08506 / Tang et al. (1993)
PH-ACO2 / L21977 / DNA / Tang et al. (1993)
PH-ACO3 / L21978 / DNA / Q08507 / Tang et al. (1993)
PH-ACO4 / L21979 / DNA / Q08508 / Tang et al. (1993)
Solanum tuberosum / ST-ACO1 / AF384820 / mRNA / Q94F66 / Nie et al. (2002)
ST-ACO2 / AF384821 / mRNA / Q94F65 / Nie et al. (2002)
ST-ACO3 / AY098939 / mRNA / Q8GVB6 / Zanetti et al. (2002)

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

Bibliography

Atkinson RG, Gunaseelan K, Wang MY, Luo L, Wang T, Norling CL, Johnston SL, Maddumage R, Schröder R, Schaffer RJ (2011) Dissecting the role of climacteric ethylene in kiwifruit (Actinidia chinensis) ripening using a 1-aminocyclopropane-1-carboxylic acid oxidase knockdown line. J Exp Bot 62:3821-3835