strigolactone-like plant hormone. Science
335(6074):1348–1351
71. Al-Babili S, Bouwmeester HJ (2015) Strigolactones, a novel carotenoid-derived plant
hormone. Annu Rev Plant Biol 66:161–186
72. Alder A, Holdermann I, Beyer P, Al-Babili S
(2008) Carotenoid oxygenases involved in
plant branching catalyse a highly specific conserved apocarotenoid cleavage reaction. Biochem J 416(2):289–296
73. Frusciante S, Diretto G, Bruno M, Ferrante P,
Pietrella M, Prado-Cabrero A, RubioMoraga A, Beyer P, Gomez-Gomez L,
Al-Babili S (2014) Novel carotenoid cleavage
dioxygenase catalyzes the first dedicated step
in saffron crocin biosynthesis. Proc Natl Acad
Sci U S A 111(33):12246–12251
74. Ahrazem O, Rubio-Moraga A, Berman J,
Capell T, Christou P, Zhu C, Go ´ mez-Go ´mez
L (2016) The carotenoid cleavage dioxygenase CCD2 catalysing the synthesis of crocetin
in spring crocuses and saffron is a plastidial
enzyme. New Phytol 209(2):650–663
75. Amengual J, Widjaja-Adhi MAK, RodriguezSantiago S, Hessel S, Golczak M,
Palczewski K, von Lintig J (2013) Two carotenoid oxygenases contribute to mammalian
provitamin a metabolism. J Biol Chem 288
(47):34081–34096
76. Babino D, Palczewski G, Widjaja-Adhi MAK,
Kiser PD, Golczak M, von Lintig J (2015)
Characterization of the role of β-carotene
9, 10-dioxygenase in macular pigment metabolism. J Biol Chem 290(41):24844–24857
77. Ohmiya A, Kishimoto S, Aida R, Yoshioka S,
Sumitomo K (2006) Carotenoid cleavage
dioxygenase (CmCCD4a) contributes to
white color formation in chrysanthemum
petals. Plant Physiol 142(3):1193–1201
78. Falchi R, Vendramin E, Zanon L, Scalabrin S,
Cipriani G, Verde I, Vizzotto G, Morgante M
(2013) Three distinct mutational mechanisms
acting on a single gene underpin the origin of
yellow flesh in peach. Plant J 76(2):175–187
79. Gonzalez-Jorge S, Ha S-H, MagallanesLundback M, Gilliland LU, Zhou A, Lipka
AE, Nguyen Y-N, Angelovici R, Lin H,
Cepela J, Little H, Buell CR, Gore MA, DellaPenna D (2013) Carotenoid cleavage dioxygenase4 is a negative regulator of β-carotene
content in Arabidopsis seeds. Plant Cell 25
(12):4812–4826
80. Vallabhaneni R, Bradbury LMT, Wurtzel ET
(2010) The carotenoid dioxygenase gene
family in maize, sorghum, and rice. Arch Biochem Biophys 504(1):104–111
81. Ilg A, Bruno M, Beyer P, Al-Babili S (2014)
Tomato carotenoid cleavage dioxygenases 1A
and 1B: relaxed double bond specificity leads
to a plenitude of dialdehydes, monoapocarotenoids and isoprenoid volatiles.
FEBS Open Bio 4:584–593
82. Ilg A, Yu Q, Schaub P, Beyer P, Al-Babili S
(2010) Overexpression of the rice carotenoid
cleavage dioxygenase 1 gene in Golden Rice
endosperm suggests apocarotenoids as substrates in planta. Planta 232(3):691–699
83. Adami M, De Franceschi P, Brandi F,
Liverani A, Giovannini D, Rosati C,
Dondini L, Tartarini S (2013) Identifying a
carotenoid cleavage dioxygenase (ccd4) gene
controlling yellow/white fruit flesh color of
peach. Plant Mol Biol Rep 31(5):1166–1175
84. Schaub P, Wuest F, Koschmieder J, Yu Q,
Virk P, Tohme J, Beyer P (2017)
Non-enzymatic β-carotene degradation in
(Provitamin A-biofortified) crop plants. J
Agric Food Chem 65(31):6588–6598
85. Ramel F, Mialoundama AS, Havaux M (2012)
Nonenzymic carotenoid oxidation and photooxidative stress signalling in plants. J Exp
Bot 64(3):799–805
86. Leenhardt F, Lyan B, Rock E, Boussard A,
Potus J, Chanliaud E, Remesy C (2006)
Genetic variability of carotenoid concentration, and lipoxygenase and peroxidase activities among cultivated wheat species and bread
wheat varieties. Eur J Agron 25(2):170–176
87. Ilg A, Beyer P, Al-Babili S (2009) Characterization of the rice carotenoid cleavage dioxygenase 1 reveals a novel route for geranial
biosynthesis. FEBS J 276(3):736–747
88. Holloway GM, Gainer JL (1988) The carotenoid crocetin enhances pulmonary oxygenation. J Appl Physiol 65(2):683–686
89. Simkin AJ, Underwood BA, Auldridge M,
Loucas HM, Shibuya K, Schmelz E, Clark
DG, Klee HJ (2004) Circadian regulation of
the PhCCD1 carotenoid cleavage dioxygenase controls emission of β-ionone, a fragrance
volatile of petunia flowers. Plant Physiol 136
(3):3504–3514
90. Ibdah M, Azulay Y, Portnoy V, Wasserman B,
Bar E, Meir A, Burger Y, Hirschberg J, Schaffer AA, Katzir N (2006) Functional characterization of CmCCD1, a carotenoid cleavage
dioxygenase from melon. Phytochemistry 67
(15):1579–1589
91. Rubio A, Rambla JL, Santaella M, Go ´ mez
MD, Orzaez D, Granell A, Go ´ mez-Go ´ mez L
(2008) Cytosolic and plastoglobule-targeted
carotenoid dioxygenases from Crocus sativus
are both involved in β-ionone release. J Biol
Chem 283(36):24816–24825
92. Ma G, Zhang L, Matsuta A, Matsutani K,
Yamawaki K, Yahata M, Wahyudi A,
20
Tianhu Sun et al.
335(6074):1348–1351
71. Al-Babili S, Bouwmeester HJ (2015) Strigolactones, a novel carotenoid-derived plant
hormone. Annu Rev Plant Biol 66:161–186
72. Alder A, Holdermann I, Beyer P, Al-Babili S
(2008) Carotenoid oxygenases involved in
plant branching catalyse a highly specific conserved apocarotenoid cleavage reaction. Biochem J 416(2):289–296
73. Frusciante S, Diretto G, Bruno M, Ferrante P,
Pietrella M, Prado-Cabrero A, RubioMoraga A, Beyer P, Gomez-Gomez L,
Al-Babili S (2014) Novel carotenoid cleavage
dioxygenase catalyzes the first dedicated step
in saffron crocin biosynthesis. Proc Natl Acad
Sci U S A 111(33):12246–12251
74. Ahrazem O, Rubio-Moraga A, Berman J,
Capell T, Christou P, Zhu C, Go ´ mez-Go ´mez
L (2016) The carotenoid cleavage dioxygenase CCD2 catalysing the synthesis of crocetin
in spring crocuses and saffron is a plastidial
enzyme. New Phytol 209(2):650–663
75. Amengual J, Widjaja-Adhi MAK, RodriguezSantiago S, Hessel S, Golczak M,
Palczewski K, von Lintig J (2013) Two carotenoid oxygenases contribute to mammalian
provitamin a metabolism. J Biol Chem 288
(47):34081–34096
76. Babino D, Palczewski G, Widjaja-Adhi MAK,
Kiser PD, Golczak M, von Lintig J (2015)
Characterization of the role of β-carotene
9, 10-dioxygenase in macular pigment metabolism. J Biol Chem 290(41):24844–24857
77. Ohmiya A, Kishimoto S, Aida R, Yoshioka S,
Sumitomo K (2006) Carotenoid cleavage
dioxygenase (CmCCD4a) contributes to
white color formation in chrysanthemum
petals. Plant Physiol 142(3):1193–1201
78. Falchi R, Vendramin E, Zanon L, Scalabrin S,
Cipriani G, Verde I, Vizzotto G, Morgante M
(2013) Three distinct mutational mechanisms
acting on a single gene underpin the origin of
yellow flesh in peach. Plant J 76(2):175–187
79. Gonzalez-Jorge S, Ha S-H, MagallanesLundback M, Gilliland LU, Zhou A, Lipka
AE, Nguyen Y-N, Angelovici R, Lin H,
Cepela J, Little H, Buell CR, Gore MA, DellaPenna D (2013) Carotenoid cleavage dioxygenase4 is a negative regulator of β-carotene
content in Arabidopsis seeds. Plant Cell 25
(12):4812–4826
80. Vallabhaneni R, Bradbury LMT, Wurtzel ET
(2010) The carotenoid dioxygenase gene
family in maize, sorghum, and rice. Arch Biochem Biophys 504(1):104–111
81. Ilg A, Bruno M, Beyer P, Al-Babili S (2014)
Tomato carotenoid cleavage dioxygenases 1A
and 1B: relaxed double bond specificity leads
to a plenitude of dialdehydes, monoapocarotenoids and isoprenoid volatiles.
FEBS Open Bio 4:584–593
82. Ilg A, Yu Q, Schaub P, Beyer P, Al-Babili S
(2010) Overexpression of the rice carotenoid
cleavage dioxygenase 1 gene in Golden Rice
endosperm suggests apocarotenoids as substrates in planta. Planta 232(3):691–699
83. Adami M, De Franceschi P, Brandi F,
Liverani A, Giovannini D, Rosati C,
Dondini L, Tartarini S (2013) Identifying a
carotenoid cleavage dioxygenase (ccd4) gene
controlling yellow/white fruit flesh color of
peach. Plant Mol Biol Rep 31(5):1166–1175
84. Schaub P, Wuest F, Koschmieder J, Yu Q,
Virk P, Tohme J, Beyer P (2017)
Non-enzymatic β-carotene degradation in
(Provitamin A-biofortified) crop plants. J
Agric Food Chem 65(31):6588–6598
85. Ramel F, Mialoundama AS, Havaux M (2012)
Nonenzymic carotenoid oxidation and photooxidative stress signalling in plants. J Exp
Bot 64(3):799–805
86. Leenhardt F, Lyan B, Rock E, Boussard A,
Potus J, Chanliaud E, Remesy C (2006)
Genetic variability of carotenoid concentration, and lipoxygenase and peroxidase activities among cultivated wheat species and bread
wheat varieties. Eur J Agron 25(2):170–176
87. Ilg A, Beyer P, Al-Babili S (2009) Characterization of the rice carotenoid cleavage dioxygenase 1 reveals a novel route for geranial
biosynthesis. FEBS J 276(3):736–747
88. Holloway GM, Gainer JL (1988) The carotenoid crocetin enhances pulmonary oxygenation. J Appl Physiol 65(2):683–686
89. Simkin AJ, Underwood BA, Auldridge M,
Loucas HM, Shibuya K, Schmelz E, Clark
DG, Klee HJ (2004) Circadian regulation of
the PhCCD1 carotenoid cleavage dioxygenase controls emission of β-ionone, a fragrance
volatile of petunia flowers. Plant Physiol 136
(3):3504–3514
90. Ibdah M, Azulay Y, Portnoy V, Wasserman B,
Bar E, Meir A, Burger Y, Hirschberg J, Schaffer AA, Katzir N (2006) Functional characterization of CmCCD1, a carotenoid cleavage
dioxygenase from melon. Phytochemistry 67
(15):1579–1589
91. Rubio A, Rambla JL, Santaella M, Go ´ mez
MD, Orzaez D, Granell A, Go ´ mez-Go ´ mez L
(2008) Cytosolic and plastoglobule-targeted
carotenoid dioxygenases from Crocus sativus
are both involved in β-ionone release. J Biol
Chem 283(36):24816–24825
92. Ma G, Zhang L, Matsuta A, Matsutani K,
Yamawaki K, Yahata M, Wahyudi A,
20
Tianhu Sun et al.