Rice Science ›› 2016, Vol. 23 ›› Issue (6): 287-296.DOI: 10.1016/j.rsci.2016.09.002
• Orginal Article • Next Articles
Chuan Tong1,2, Lei Liu3, L. E. Waters Daniel3, Jin-song Bao1
Received:
2016-07-25
Accepted:
2016-09-22
Online:
2016-12-12
Published:
2016-08-10
Chuan Tong, Lei Liu, L. E. Waters Daniel, Jin-song Bao. Association Mapping and Marker Development of Genes for Starch Lysophospholipid Synthesis in Rice[J]. Rice Science, 2016, 23(6): 287-296.
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Fig. 1. Conceivable biosynthetic pathways of phospholipids in cereals. Drawn based on Kinney (1993), D’Arrigo and Servi (2010) and Liu et al (2013). E, Ethanolamine; ME, Methylethanolamine; DME, Dimethylethanolamine; IP3, inositol 1,4,5-triphosphate; LPA, Lysophosphatidic acid; C, Choline; P, Phosphate; CDP, Cytidinediphosphate; PE, Phosphatidylethanolamine; PME, Phosphatidylmethylethanolamine; PDME, Phosphatidyldimethyle- thanolamine; PC, Phosphatidylcholine; PS, Phosphatidylserine; PI, Phosphatidylinositol; PIP, Phosphatidylinositol phosphate; PIP2, Phosphati- dylinositolbisphosphate; PGP, Phosphoglycerol phosphate; PG, Phosphatidylglycerol; DPG, Diphosphatidylglycerol; , Glycerol-3-phosphate acyltransferase; , 1-monoacylglycerol-3-phosphate acyltransferase; , CDP-diacylglycerol synthase (CTP: phosphatidatecytidylyltransferase); , Phosphatidatephosphohydrolase; , PI synthase (CDP-diacylglycerol: myo-inositol phosphatidyltransferase); , PI 4-kinase (ATP: phosphati- dylinositol-4-phosphotransferase); , PIP kinase (ATP: phosphatidylinositol 4-phosphate 5-phosphotransferase); , PGP synthase (CDP-diacylgly- cerolphosphatidyltransferase); , PGP phosphatase (phosphatidylglycerol-phosphate phosphohydrolase); , CDP diacylglycerolphosphatidly- transerase; , PS synthase (CDP-diacylglycerol: L-serine O-phosphatidyltransferase); , PS decarboxylase; , PE N-methyltransferase; , Phospholipid N-methyltransferase; , Aminoalcoholphosphotransferase; , Ethanolaminephosphotransferase (CDP-ethanolamine: 1,2-diacylglycerol cytidylyltransferase); , Ethanolamine phosphate cytidylyltransferase (CTP: ethanolamine phosphate cytidylyltransferase); , Ethanolamine kinase (ATP: ethanolamine phosphotransferase); , Cholinephosphotransferase (CDP-choline: 1,2-diacylglycerol cytidylyltransferase); , Choline phosphate cytidylyltransferase (CTP: choline phosphate cytidylyltransferase); , Choline kinase (ATP: choline phosphotransferase); , Phospholipase D (PLD) (Phosphatidylcholinephosphatidohydrolase); , Phospholipase C (PLC); , Diacylglycerol (DAG) kinase; , Phospholipase A2 (PLA2).
Trait | Year | Model | QTL | Chr | Position a (bp) | P-value | Major allele | Minor allele | Minor allele frequency | Allelic effect (R2) | |
LPC16:0 | 2011 | K | qC160-6-1 | 6 | 26 685 967 | 4.72 × 10-3 | C | T | 0.30 | 0.8011 | |
2012 | K | qC160-6-2 | 6 | 3 235 560 | 4.41 × 10-3 | G | A | 0.25 | 0.5573 | ||
qC160-8 | 8 | 8 481 084 | 3.64 × 10-3 | A | G | 0.40 | 0.5872 | ||||
LPC18:1 | 2012 | Q+K | qC181-2 | 2 | 14 522 544 | 3.15 × 10-3 | G | A | 0.20 | 0.8346 | |
qC181-1 | 1 | 27 729 601 | 4.20 × 10-3 | C | T | 0.30 | 0.8107 | ||||
LPC18:2 | 2011 | K | qC182-9 | 9 | 15 125 638 | 4.37 × 10-3 | C | T | 0.20 | 0.5585 | |
2012 | K | qC182-11 | 11 | 17 847 796 | 4.07 × 10-3 | A | T | 0.30 | 0.5698 | ||
LPC18:3 | 2011 | K | qC183-1 | 1 | 23 517 183 | 3.27 × 10-3 | A | C | 0.25 | 0.6047 | |
2012 | K | qC183-1 | 1 | 23 517 183 | 4.89 × 10-3 | A | C | 0.25 | 0.5411 | ||
TLPC | 2011 | ANOVA | qC-5 | 5 | 23 465 186 | 4.20 × 10-3 | G | A | 0.25 | 0.5647 | |
qC-9 | 9 | 15 125 638 | 2.62 × 10-3 | C | T | 0.20 | 0.6409 | ||||
qC-12 | 12 | 21 175 392 | 3.73 × 10-3 | T | A | 0.25 | 0.5835 | ||||
2012 | K | qC-10 | 10 | 5 339 258 | 4.36 × 10-3 | G | A | 0.25 | 0.5589 | ||
LPE16:0 | 2011 | ANOVA | qE160-1 | 1 | 6 971 525 | 3.33 × 10-3 | G | A | 0.25 | 0.6016 | |
LPE18:1 | 2011 | Q+K | qE181-2 | 2 | 14 522 544 | 3.26 × 10-3 | G | A | 0.20 | 0.7802 | |
2012 | Q+K | qE181-2 | 2 | 14 522 544 | 2.17 × 10-3 | G | A | 0.20 | 0.8364 | ||
LPE18:2 | 2011 | K | qE182-1 | 1 | 23 585 360 | 3.23 × 10-3 | C | T | 0.25 | 0.6064 | |
qE182-4 | 4 | 31 271 474 | 4.23 × 10-3 | T | C | 0.20 | 0.5637 | ||||
qE182-11 | 11 | 17 943 118 | 3.82 × 10-3 | T | A | 0.35 | 0.5798 | ||||
LPE18:3 | 2011 | K | qE183-1 | 1 | 23 517 183 | 4.27 × 10-3 | A | C | 0.25 | 0.5623 | |
2012 | K | qE183-1 | 1 | 23 517 183 | 4.33 × 10-3 | A | C | 0.25 | 0.5600 | ||
TLPE | 2011 | ANOVA | qE-10 | 10 | 5 339 258 | 4.69 × 10-3 | G | A | 0.25 | 0.5477 | |
TLPL | 2011 | ANOVA | qL-9 | 9 | 15 125 638 | 2.92 × 10-3 | C | T | 0.20 | 0.6229 | |
qL-10 | 10 | 5 339 258 | 4.67 × 10-3 | G | A | 0.25 | 0.5482 | ||||
qL-12 | 12 | 21 175 392 | 4.93 × 10-3 | T | A | 0.25 | 0.5399 | ||||
2012 | K | qL-10 | 10 | 5 339 258 | 4.19 × 10-3 | G | A | 0.25 | 0.5649 | ||
LPC14:0, 1-myristoyl-2-hydroxy-sn-glycero-3-phosphocholine; LPC16:0, 1-palmitoyl-2-hydroxy-sn-glycero-3-phosphocholine; LPC18:1, 1-oleoyl- 2-hydroxy-sn-glycero-3-phosphocholine; LPC18:2, 1-linoleoyl-2-hydroxy-sn-glycero-3-phosphocholine; LPC18:3, 1-linolenoyl-2-hydroxy-sn- glycero-3-phosphocholine; LPE14:0, 1-myristoyl-2-hydroxy-sn-glycero-3-phosphoethanolamine; LPE16:0, 1-palmitoyl-2-hydroxy-sn-glycero-3- phosphoethanolamine; LPE18:1, 1-oleoyl-2-hydroxy-sn-glycero-3-phosphoethanolamine; LPE18:2, 1-linoleoyl-2-hydroxy-sn-glycero-3-phosphoethanolamine; LPE18:3, 1-linolenoyl-2-hydroxy-sn-glycero-3-phosphoethanolamine; TLPC, Total lysophosphatidylcholine; TLPE, Total lysophosphatidylethanolamine; TLPL, Total lysophospholipid; Q, Population structure; K, Kinship; ANOVA, Analysis of variance; Chr, Chromosome. a, Position in base pairs for the leading SNP of rice sequence. |
Table 1 Genome-wide significantly associated QTLs for rice lysophospholipids (LPLs)
Trait | Year | Model | QTL | Chr | Position a (bp) | P-value | Major allele | Minor allele | Minor allele frequency | Allelic effect (R2) | |
LPC16:0 | 2011 | K | qC160-6-1 | 6 | 26 685 967 | 4.72 × 10-3 | C | T | 0.30 | 0.8011 | |
2012 | K | qC160-6-2 | 6 | 3 235 560 | 4.41 × 10-3 | G | A | 0.25 | 0.5573 | ||
qC160-8 | 8 | 8 481 084 | 3.64 × 10-3 | A | G | 0.40 | 0.5872 | ||||
LPC18:1 | 2012 | Q+K | qC181-2 | 2 | 14 522 544 | 3.15 × 10-3 | G | A | 0.20 | 0.8346 | |
qC181-1 | 1 | 27 729 601 | 4.20 × 10-3 | C | T | 0.30 | 0.8107 | ||||
LPC18:2 | 2011 | K | qC182-9 | 9 | 15 125 638 | 4.37 × 10-3 | C | T | 0.20 | 0.5585 | |
2012 | K | qC182-11 | 11 | 17 847 796 | 4.07 × 10-3 | A | T | 0.30 | 0.5698 | ||
LPC18:3 | 2011 | K | qC183-1 | 1 | 23 517 183 | 3.27 × 10-3 | A | C | 0.25 | 0.6047 | |
2012 | K | qC183-1 | 1 | 23 517 183 | 4.89 × 10-3 | A | C | 0.25 | 0.5411 | ||
TLPC | 2011 | ANOVA | qC-5 | 5 | 23 465 186 | 4.20 × 10-3 | G | A | 0.25 | 0.5647 | |
qC-9 | 9 | 15 125 638 | 2.62 × 10-3 | C | T | 0.20 | 0.6409 | ||||
qC-12 | 12 | 21 175 392 | 3.73 × 10-3 | T | A | 0.25 | 0.5835 | ||||
2012 | K | qC-10 | 10 | 5 339 258 | 4.36 × 10-3 | G | A | 0.25 | 0.5589 | ||
LPE16:0 | 2011 | ANOVA | qE160-1 | 1 | 6 971 525 | 3.33 × 10-3 | G | A | 0.25 | 0.6016 | |
LPE18:1 | 2011 | Q+K | qE181-2 | 2 | 14 522 544 | 3.26 × 10-3 | G | A | 0.20 | 0.7802 | |
2012 | Q+K | qE181-2 | 2 | 14 522 544 | 2.17 × 10-3 | G | A | 0.20 | 0.8364 | ||
LPE18:2 | 2011 | K | qE182-1 | 1 | 23 585 360 | 3.23 × 10-3 | C | T | 0.25 | 0.6064 | |
qE182-4 | 4 | 31 271 474 | 4.23 × 10-3 | T | C | 0.20 | 0.5637 | ||||
qE182-11 | 11 | 17 943 118 | 3.82 × 10-3 | T | A | 0.35 | 0.5798 | ||||
LPE18:3 | 2011 | K | qE183-1 | 1 | 23 517 183 | 4.27 × 10-3 | A | C | 0.25 | 0.5623 | |
2012 | K | qE183-1 | 1 | 23 517 183 | 4.33 × 10-3 | A | C | 0.25 | 0.5600 | ||
TLPE | 2011 | ANOVA | qE-10 | 10 | 5 339 258 | 4.69 × 10-3 | G | A | 0.25 | 0.5477 | |
TLPL | 2011 | ANOVA | qL-9 | 9 | 15 125 638 | 2.92 × 10-3 | C | T | 0.20 | 0.6229 | |
qL-10 | 10 | 5 339 258 | 4.67 × 10-3 | G | A | 0.25 | 0.5482 | ||||
qL-12 | 12 | 21 175 392 | 4.93 × 10-3 | T | A | 0.25 | 0.5399 | ||||
2012 | K | qL-10 | 10 | 5 339 258 | 4.19 × 10-3 | G | A | 0.25 | 0.5649 | ||
LPC14:0, 1-myristoyl-2-hydroxy-sn-glycero-3-phosphocholine; LPC16:0, 1-palmitoyl-2-hydroxy-sn-glycero-3-phosphocholine; LPC18:1, 1-oleoyl- 2-hydroxy-sn-glycero-3-phosphocholine; LPC18:2, 1-linoleoyl-2-hydroxy-sn-glycero-3-phosphocholine; LPC18:3, 1-linolenoyl-2-hydroxy-sn- glycero-3-phosphocholine; LPE14:0, 1-myristoyl-2-hydroxy-sn-glycero-3-phosphoethanolamine; LPE16:0, 1-palmitoyl-2-hydroxy-sn-glycero-3- phosphoethanolamine; LPE18:1, 1-oleoyl-2-hydroxy-sn-glycero-3-phosphoethanolamine; LPE18:2, 1-linoleoyl-2-hydroxy-sn-glycero-3-phosphoethanolamine; LPE18:3, 1-linolenoyl-2-hydroxy-sn-glycero-3-phosphoethanolamine; TLPC, Total lysophosphatidylcholine; TLPE, Total lysophosphatidylethanolamine; TLPL, Total lysophospholipid; Q, Population structure; K, Kinship; ANOVA, Analysis of variance; Chr, Chromosome. a, Position in base pairs for the leading SNP of rice sequence. |
Fig. 2. Location of QTLs for rice starch lysophospholipids (LPLs) on chromosomes (Chr). C160, C181, C182, C183, E160, E181, E182, E183, C, E and L in the QTLs represent LPC16:0, LPC18:1, LPC18:2, LPC18:3, LPE16:0, LPE18:1, LPE18:2, LPE18:3, total lysophosphatidylcholine, total lysophosphatidylethanolamine and total lysophospholipid, respectively.
Fig. 4. Part sequence alignments of AAPT and PLA2 genes. A, InDel found in AAPT gene among G01-G20; B, Single nucleotide polymorphism found in PLA2 gene among G01-G20. AAPT, Aminoalcoholphosphotransferase; PLA2, Phospholipase A2.
Primer | Type | Sequence (5′-3′) | PCR product (bp) | Restriction enzyme | Enzyme digestion product (bp) |
AAPT1-F | InDel | CCAGCCTTGTTTCAATACCTG | 134/127 | - | - |
AAPT1-R | AAATGTAGGAAGTTTTTACTTGC | ||||
AAPT2-F | dCAPS | AAGAGCAAGTAAAAACTTCCTAAATT | 222 | ApoI | 22, 200 |
AAPT2-R | GATACAAATGCCCAAATACCA | ||||
AAPT3-F | dCAPS | CAAAGATCAATGCTGGGTAATTTC | 184 | SphI | 22, 162 |
AAPT3-R | AGGTAAATCAGTTCACCTGTGCA | ||||
PLD1-F | dCAPS | CATCCTGCACTAAAAACAGTTGAAT | 214 | HinfI | 22, 192 |
PLD1-R | TGCACAACACCAGAGCCCCACC | ||||
PLD2-F | dCAPS | CCTCCCAAAGTTTAGGCGGAAAAGGCC | 187 | HpaII | 27, 160 |
PLD2-R | TCAAAGCTCACAATAGCAGAATA | ||||
PLA21-F | dCAPS | TTCCTATTGTTTCTTCCTCCCTCTT | 230 | HinfI | 20, 210 |
PLA21-R | GAAAAAACAAAATTAAAAAAGAGT | ||||
dCAPS, Development of derived cleaved amplified polymorphic sequences. Underlined letter means the mismatch base. |
Table 2 Primers for enzyme digestion of several single nucleotide polymorphisms
Primer | Type | Sequence (5′-3′) | PCR product (bp) | Restriction enzyme | Enzyme digestion product (bp) |
AAPT1-F | InDel | CCAGCCTTGTTTCAATACCTG | 134/127 | - | - |
AAPT1-R | AAATGTAGGAAGTTTTTACTTGC | ||||
AAPT2-F | dCAPS | AAGAGCAAGTAAAAACTTCCTAAATT | 222 | ApoI | 22, 200 |
AAPT2-R | GATACAAATGCCCAAATACCA | ||||
AAPT3-F | dCAPS | CAAAGATCAATGCTGGGTAATTTC | 184 | SphI | 22, 162 |
AAPT3-R | AGGTAAATCAGTTCACCTGTGCA | ||||
PLD1-F | dCAPS | CATCCTGCACTAAAAACAGTTGAAT | 214 | HinfI | 22, 192 |
PLD1-R | TGCACAACACCAGAGCCCCACC | ||||
PLD2-F | dCAPS | CCTCCCAAAGTTTAGGCGGAAAAGGCC | 187 | HpaII | 27, 160 |
PLD2-R | TCAAAGCTCACAATAGCAGAATA | ||||
PLA21-F | dCAPS | TTCCTATTGTTTCTTCCTCCCTCTT | 230 | HinfI | 20, 210 |
PLA21-R | GAAAAAACAAAATTAAAAAAGAGT | ||||
dCAPS, Development of derived cleaved amplified polymorphic sequences. Underlined letter means the mismatch base. |
Accession | AAPT1 | AAPT2 | AAPT3 | PLD1 | PLD2 | PLA21 | Accession | AAPT1 | AAPT2 | AAPT3 | PLD1 | PLD2 | PLA21 |
G01 | D | T | A | C | G | G | G18 | I | A | G | C | C | G |
G02 | D | T | A | C | G | G | G19 | D | T | A | C | G | T |
G03 | D | T | A | A | C | T | G20 | I | A | G | A | C | T |
G04 | D | T | A | A | C | G | R01 | D | T | A | C | C | G |
G05 | D | T | A | C | C | T | R02 | D | T | A | C | C | G |
G06 | D | T | A | C | G | G | R03 | D | T | A | C | G | T |
G07 | D | T | A | C | G | G | R04 | D | T | A | C | C | G |
G08 | D | T | A | C | C | T | R05 | D | T | A | C | C | T |
G09 | D | T | A | C | G | G | R06 | D | T | A | C | C | G |
G10 | D | T | A | A | C | T | R07 | D | T | A | C | G | G |
G11 | D | T | A | C | G | G | R08 | I | A | G | C | C | G |
G12 | D | T | A | C | C | T | R09 | D | T | A | C | C | T |
G13 | D | T | A | C | C | T | R10 | I | A | G | C | C | T |
G14 | I | A | G | C | C | T | R11 | D | T | A | C | C | T |
G15 | D | T | A | C | C | G | R12 | D | T | A | C | C | T |
G16 | D | T | A | C | G | G | R13 | I | A | G | C | C | T |
G17 | I | A | G | C | C | G | |||||||
AAPT, Aminoalcoholphosphotransferase; PLD, Phospholipase D; PLA2, Phospholipase A2; I, Insertion; D, Deletion. |
Table 3 Summary of alleles of three candidate genes.
Accession | AAPT1 | AAPT2 | AAPT3 | PLD1 | PLD2 | PLA21 | Accession | AAPT1 | AAPT2 | AAPT3 | PLD1 | PLD2 | PLA21 |
G01 | D | T | A | C | G | G | G18 | I | A | G | C | C | G |
G02 | D | T | A | C | G | G | G19 | D | T | A | C | G | T |
G03 | D | T | A | A | C | T | G20 | I | A | G | A | C | T |
G04 | D | T | A | A | C | G | R01 | D | T | A | C | C | G |
G05 | D | T | A | C | C | T | R02 | D | T | A | C | C | G |
G06 | D | T | A | C | G | G | R03 | D | T | A | C | G | T |
G07 | D | T | A | C | G | G | R04 | D | T | A | C | C | G |
G08 | D | T | A | C | C | T | R05 | D | T | A | C | C | T |
G09 | D | T | A | C | G | G | R06 | D | T | A | C | C | G |
G10 | D | T | A | A | C | T | R07 | D | T | A | C | G | G |
G11 | D | T | A | C | G | G | R08 | I | A | G | C | C | G |
G12 | D | T | A | C | C | T | R09 | D | T | A | C | C | T |
G13 | D | T | A | C | C | T | R10 | I | A | G | C | C | T |
G14 | I | A | G | C | C | T | R11 | D | T | A | C | C | T |
G15 | D | T | A | C | C | G | R12 | D | T | A | C | C | T |
G16 | D | T | A | C | G | G | R13 | I | A | G | C | C | T |
G17 | I | A | G | C | C | G | |||||||
AAPT, Aminoalcoholphosphotransferase; PLD, Phospholipase D; PLA2, Phospholipase A2; I, Insertion; D, Deletion. |
Fig. 5. Polymorphism of InDel and simple nucleotide polymorphisms in AAPT, PLD and PLA2 genes in rice accessions G01-G20 and R01-R13. AAPT, Aminoalcoholphosphotransferase; PLD, Phospholipase D; PLA2, Phospholipase A2. Lanes from left to right in each part are marker, G01-G20 and R01-R13, respectively.
Gene | Marker | Trait | Non-waxy accession (31) | All rice accession (33) | QTL | |||
p_Marker | R2_Marker | p_Marker | R2_Marker | |||||
PLD | PLD1 | LPC16:0 | 0.0149 | 0.1876 | 0.0984 | 0.0856 | qC160-6-1 | |
PLA2 | PLA21 | LPC18:2 | 0.0902 | 0.0958 | 0.0277 | 0.1468 | qC182-11, qE182-11 | |
PLD, Phospholipase D; PLA2, Phospholipase A2. |
Table 4 Marker loci associated with starch lysophospholipids (LPLs) traits detected with analysis of variance (ANOVA) model in 31 non-waxy and all the 33 rice accessions.
Gene | Marker | Trait | Non-waxy accession (31) | All rice accession (33) | QTL | |||
p_Marker | R2_Marker | p_Marker | R2_Marker | |||||
PLD | PLD1 | LPC16:0 | 0.0149 | 0.1876 | 0.0984 | 0.0856 | qC160-6-1 | |
PLA2 | PLA21 | LPC18:2 | 0.0902 | 0.0958 | 0.0277 | 0.1468 | qC182-11, qE182-11 | |
PLD, Phospholipase D; PLA2, Phospholipase A2. |
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39 | (Managing Editor: Li Guan) |
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