24. Camagna M, Grundmann A, B€ ar C,
Koschmieder J, Beyer P, Welsch R (2019)
Enzyme fusion removes competition for geranylgeranyl diphosphate in carotenogenesis.
Plant Physiol 179(3):1013–1027
25. Li F, Tzfadia O, Wurtzel ET (2009) The phytoene synthase gene family in the grasses: subfunctionalization provides tissue-specific
control of carotenogenesis. Plant Signal
Behav 4(3):208–211
26. Giuliano G (2017) Provitamin a biofortification of crop plants: a gold rush with many
miners. Curr Opin Biotechnol 44:169–180
27. Chen Y, Li F, Wurtzel ET (2010) Isolation
and characterization of the Z-ISO gene
encoding a missing component of carotenoid
biosynthesis in plants. Plant Physiol 153
(1):66–79
28. Carol P, Kuntz M (2001) A plastid terminal
oxidase comes to light: implications for carotenoid biosynthesis and chlororespiration.
Trends Plant Sci 6(1):31–36
29. Hunter CT, Saunders JW, MagallanesLundback M, Christensen SA, Willett D, Stinard PS, Li QB, Lee K, DellaPenna D, Koch
KE (2018) Maize w3 disrupts homogentisate
solanesyl transferase (ZmHst) and reveals a
plastoquinone-9 independent path for phytoene desaturation and tocopherol accumulation in kernels. Plant J 93(5):799–813
30. Beltra ´n J, Kloss B, Hosler JP, Geng J, Liu A,
Modi A, Dawson JH, Sono M, Shumskaya M,
Ampomah-Dwamena C, Love JD, Wurtzel
ET (2015) Control of carotenoid biosynthesis
through a heme-based cis-trans isomerase.
Nat Chem Biol 11(8):598–605
31. Yu Q, Ghisla S, Hirschberg J, Mann V, Beyer
P (2011) Plant carotene cis-trans isomerase
crtiso a new member of the fadred-dependent
flavoproteins catalyzing non-redox reactions.
J Biol Chem 286(10):8666–8676
32. Bai L, Kim EH, DellaPenna D, Brutnell TP
(2009) Novel lycopene epsilon cyclase activities in maize revealed through perturbation
of carotenoid biosynthesis. Plant J 59
(4):588–599
33. Harjes CE, Rocheford TR, Bai L, Brutnell TP,
Kandianis CB, Sowinski SG, Stapleton AE,
Vallabhaneni R, Williams M, Wurtzel ET
(2008) Natural genetic variation in lycopene
epsilon cyclase tapped for maize biofortification. Science 319(5861):330–333
34. Kim J, Smith JJ, Tian L, DellaPenna D (2009)
The evolution and function of carotenoid
hydroxylases in Arabidopsis. Plant Cell
Physiol 50(3):463–479
35. Jahns P, Holzwarth AR (2012) The role of the
xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys
Acta 1817(1):182–193
36. Neuman H, Galpaz N, Cunningham FX,
Zamir D, Hirschberg J (2014) The tomato
mutation nxd1 reveals a gene necessary for
neoxanthin biosynthesis and demonstrates
that violaxanthin is a sufficient precursor for
abscisic acid biosynthesis. Plant J 78(1):80–93
37. Ruiz-Sola MA ´ , Rodrı ´guez-Concepcio ´n M
(2012) Carotenoid biosynthesis in Arabidopsis: a colorful pathway. Arabidopsis Book 10:
e0158
38. Al-Babili S, Jv L, Haubruck H, Beyer P
(1996) A novel, soluble form of phytoene
desaturase from Narcissus pseudonarcissus
chromoplasts is Hsp70-complexed and competent for flavinylation, membrane association
and enzymatic activation. Plant J 9
(5):601–612
39. Lopez AB, Yang Y, Thannhauser TW, Li L
(2008) Phytoene desaturase is present in a
large protein complex in the plastid membrane. Physiol Plant 133(2):190–198
40. Quinlan RF, Shumskaya M, Bradbury LMT,
Beltra ´n J, Ma C, Kennelly EJ, Wurtzel ET
(2012) Synergistic interactions between carotene ring hydroxylases drive lutein formation
in plant carotenoid biosynthesis. Plant Physiol
160(1):204–214
41. Pulido P, Toledo-Ortiz G, Phillips MA,
Wright LP, Rodrı ´guez-Concepcio ´n M
(2013) Arabidopsis J-protein J20 delivers the
first enzyme of the plastidial isoprenoid pathway to protein quality control. Plant Cell 25
(10):4183–4194
42. Pulido P, Llamas E, Llorente B, Ventura S,
Wright LP, Rodrı ´guez-Concepcio ´n M
(2016) Specific Hsp100 chaperones determine the fate of the first enzyme of the plastidial isoprenoid pathway for either refolding
or degradation by the stromal Clp protease in
Arabidopsis. PLoS Genet 12(1):e1005824
43. Zhou X, Welsch R, Yang Y, A ´ lvarez D,
Riediger M, Yuan H, Fish T, Liu J, Thannhauser TW, Li L (2015) Arabidopsis OR proteins are the major posttranscriptional
regulators of phytoene synthase in controlling
carotenoid biosynthesis. Proc Natl Acad Sci U
S A 112(11):3558–3563
44. Park S, Kim HS, Jung YJ, Kim SH, Ji CY,
Wang Z, Jeong JC, Lee H-S, Lee SY, Kwak
S-S (2016) Orange protein has a role in phytoene synthase stabilization in sweetpotato.
Sci Rep 6
18
Tianhu Sun et al.
Koschmieder J, Beyer P, Welsch R (2019)
Enzyme fusion removes competition for geranylgeranyl diphosphate in carotenogenesis.
Plant Physiol 179(3):1013–1027
25. Li F, Tzfadia O, Wurtzel ET (2009) The phytoene synthase gene family in the grasses: subfunctionalization provides tissue-specific
control of carotenogenesis. Plant Signal
Behav 4(3):208–211
26. Giuliano G (2017) Provitamin a biofortification of crop plants: a gold rush with many
miners. Curr Opin Biotechnol 44:169–180
27. Chen Y, Li F, Wurtzel ET (2010) Isolation
and characterization of the Z-ISO gene
encoding a missing component of carotenoid
biosynthesis in plants. Plant Physiol 153
(1):66–79
28. Carol P, Kuntz M (2001) A plastid terminal
oxidase comes to light: implications for carotenoid biosynthesis and chlororespiration.
Trends Plant Sci 6(1):31–36
29. Hunter CT, Saunders JW, MagallanesLundback M, Christensen SA, Willett D, Stinard PS, Li QB, Lee K, DellaPenna D, Koch
KE (2018) Maize w3 disrupts homogentisate
solanesyl transferase (ZmHst) and reveals a
plastoquinone-9 independent path for phytoene desaturation and tocopherol accumulation in kernels. Plant J 93(5):799–813
30. Beltra ´n J, Kloss B, Hosler JP, Geng J, Liu A,
Modi A, Dawson JH, Sono M, Shumskaya M,
Ampomah-Dwamena C, Love JD, Wurtzel
ET (2015) Control of carotenoid biosynthesis
through a heme-based cis-trans isomerase.
Nat Chem Biol 11(8):598–605
31. Yu Q, Ghisla S, Hirschberg J, Mann V, Beyer
P (2011) Plant carotene cis-trans isomerase
crtiso a new member of the fadred-dependent
flavoproteins catalyzing non-redox reactions.
J Biol Chem 286(10):8666–8676
32. Bai L, Kim EH, DellaPenna D, Brutnell TP
(2009) Novel lycopene epsilon cyclase activities in maize revealed through perturbation
of carotenoid biosynthesis. Plant J 59
(4):588–599
33. Harjes CE, Rocheford TR, Bai L, Brutnell TP,
Kandianis CB, Sowinski SG, Stapleton AE,
Vallabhaneni R, Williams M, Wurtzel ET
(2008) Natural genetic variation in lycopene
epsilon cyclase tapped for maize biofortification. Science 319(5861):330–333
34. Kim J, Smith JJ, Tian L, DellaPenna D (2009)
The evolution and function of carotenoid
hydroxylases in Arabidopsis. Plant Cell
Physiol 50(3):463–479
35. Jahns P, Holzwarth AR (2012) The role of the
xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys
Acta 1817(1):182–193
36. Neuman H, Galpaz N, Cunningham FX,
Zamir D, Hirschberg J (2014) The tomato
mutation nxd1 reveals a gene necessary for
neoxanthin biosynthesis and demonstrates
that violaxanthin is a sufficient precursor for
abscisic acid biosynthesis. Plant J 78(1):80–93
37. Ruiz-Sola MA ´ , Rodrı ´guez-Concepcio ´n M
(2012) Carotenoid biosynthesis in Arabidopsis: a colorful pathway. Arabidopsis Book 10:
e0158
38. Al-Babili S, Jv L, Haubruck H, Beyer P
(1996) A novel, soluble form of phytoene
desaturase from Narcissus pseudonarcissus
chromoplasts is Hsp70-complexed and competent for flavinylation, membrane association
and enzymatic activation. Plant J 9
(5):601–612
39. Lopez AB, Yang Y, Thannhauser TW, Li L
(2008) Phytoene desaturase is present in a
large protein complex in the plastid membrane. Physiol Plant 133(2):190–198
40. Quinlan RF, Shumskaya M, Bradbury LMT,
Beltra ´n J, Ma C, Kennelly EJ, Wurtzel ET
(2012) Synergistic interactions between carotene ring hydroxylases drive lutein formation
in plant carotenoid biosynthesis. Plant Physiol
160(1):204–214
41. Pulido P, Toledo-Ortiz G, Phillips MA,
Wright LP, Rodrı ´guez-Concepcio ´n M
(2013) Arabidopsis J-protein J20 delivers the
first enzyme of the plastidial isoprenoid pathway to protein quality control. Plant Cell 25
(10):4183–4194
42. Pulido P, Llamas E, Llorente B, Ventura S,
Wright LP, Rodrı ´guez-Concepcio ´n M
(2016) Specific Hsp100 chaperones determine the fate of the first enzyme of the plastidial isoprenoid pathway for either refolding
or degradation by the stromal Clp protease in
Arabidopsis. PLoS Genet 12(1):e1005824
43. Zhou X, Welsch R, Yang Y, A ´ lvarez D,
Riediger M, Yuan H, Fish T, Liu J, Thannhauser TW, Li L (2015) Arabidopsis OR proteins are the major posttranscriptional
regulators of phytoene synthase in controlling
carotenoid biosynthesis. Proc Natl Acad Sci U
S A 112(11):3558–3563
44. Park S, Kim HS, Jung YJ, Kim SH, Ji CY,
Wang Z, Jeong JC, Lee H-S, Lee SY, Kwak
S-S (2016) Orange protein has a role in phytoene synthase stabilization in sweetpotato.
Sci Rep 6
18
Tianhu Sun et al.