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Acta Agronomica Sinica ›› 2019, Vol. 45 ›› Issue (5): 662-675.doi: 10.3724/SP.J.1006.2019.82049

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Phenotypic identification and gene mapping of temperature-sensitive green- revertible albino mutant tsa2 in rice (Oryza sativa L.)

Li-Na SHANG,Xin-Long CHEN,Sheng-Nan MI,Gang WEI,Ling WANG,Ya-Yi ZHANG,Ting LEI,Yong-Xin LIN,Lan-Jie HUANG,Mei-Dan ZHU,Nan WANG()   

  1. Rice Research Institute, Southwest University / Academy of Agricultural Sciences, Southwest University, Chongqing 400715, China
  • Received:2018-10-10 Accepted:2019-01-12 Online:2019-05-12 Published:2019-02-12
  • Contact: Nan WANG E-mail:wangnan_xndx@126.com
  • Supported by:
    This study was supported by the National Natural Science Foundation of China(31771750);Basic Research and Frontier Exploration Project in Chongqing(cstc2018jcyjAX0424);the Graduate Research and Innovation Project in Chongqing(CYS18084)

Abstract:

Temperature-sensitive leaf color mutants of rice are ideal materials in studies on photosynthesis, chloroplast structure and function, and chloroplast development. A temperature-sensitive green-revertible albino mutant (tsa2) with genetically stable mutational traits was screened out from the progeny of ethyl methane sulfonate (EMS) treated indica three-line maintainer line Xinong 1B. The wild type seedlings had normal phenotype at 22°C, while the mutant tsa2 had completely albino leaves and about 40% of albino seedlings died at the seedling stage; the photosynthetic pigment contents and photosynthetic rate of surviving albino seedlings decreased significantly, and the main agronomic traits were significantly lower than those of the wild type at maturity stage. When germinated at 28°C, tsa2 showed light-green leaves with white streaks and significantly lower photosynthetic pigment contents than the wild type, while a small difference of photosynthetic rate and main agronomic traits between the tsa2 and the wild type. No significant difference in leaves was observed between tsa2 and the wild type when seedlings germinated at 32°C. Transmission electron microscope observation revealed that the albino leaves of tsa2 demonstrated abnormal chloroplast development (without differentiated grana and granum lamella) or without chloroplast at 22°C and completely developed chloroplasts in partial mesophyll cells at 28°C, and normal number and morphology of mesophyll cells compared with wild type at 32°C. The analysis of qRT-PCR indicated that genes related to partial photosynthetic pigment metabolism pathways, chloroplast development and photosynthesis expressed in tsa2 to a varying degrees compared with these of the wild type. Genetic analysis suggested that mutational phenotype of tsa2 was controlled by a single recessive nuclear gene, TSA2, which was finally mapped between SSR markers S5-57 and S5-119 on chromosome 5, with a physical distance of 718 kb. These results lay a foundation for the research on genetic improvement and the mechanism explanation of chloroplast development affected by temperature in rice (Oryza sativa L.).

Key words: rice (Oryza sativa L.), temperature-sensitive, green-revertible albino, chloroplast ultrastructure, gene mapping

Fig. 1

Phenotypes of the wild type (WT) and tsa2 mutant A, B, C: seedling stage (A), tillering stage (B), and mature stage (C) of the wild type (WT) and tsa2 mutant seedled at a daily average temperature of 22°C; D, E, F: seedling stage (D), tillering stage (E), and mature stage (F) of the wild type (WT) and tsa2 mutant seedled at a daily average temperature of 28°C; G, H, I, J, K, L: corresponding to the leaves in A, B, C, D, E, F, respectively. 1, 2, 3, and 4 in the figures H, I, K, and L represent the first, second, third, and fourth fully expanded leaves from topmost leaf, respectively. A and D, Bar = 2 cm; B and E, Bar = 6 cm; C and F, Bar = 13 cm; G-L, Bar = 0.7 cm."

Fig. 2

Photosynthetic parameters of the wild type (WT) and tsa2 mutant seeded under different field temperature conditions A: net photosynthetic rate (Pn); B: stomatal conductance (Gs); C: intercellular CO2 concentration (Ci); D: transpiration rate (Tr); **: significant difference at P < 0.01 by t-test."

Fig. 3

Agronomic traits of the wild type (WT) and tsa2 mutant seeded under different field temperature conditions A: plant height (cm); B: panicle length (cm); C: tiller number; D: effective panicle number; E: grain number per panicle; F: filled grain number per panicle; G: 1000-grain weight (g); H: seed setting rate (%); *: significant difference at P<0.05 by t-test; **: significant difference at P<0.01 by t-test."

Fig. 4

Phenotype and photosynthetic pigment content of the wild type (WT) and tsa2 mutant seedlings under different temperature conditions A, B, C: twenty-two days old seedings of the wild type (WT) and tsa2 mutant seeded under 22°C (A), 28°C (B), and 32°C (C), respectively; D: photosynthetic pigment contents of the wild type (WT) and tsa2 mutant seedlings seeded under different temperature conditions; **: significant difference at P < 0.01 by t-test. A, B, and C, Bar = 2.5 cm."

Fig. 5

Ultrastructure of chloroplasts in mesophyll cells of the wild type (WT) and tsa2 mutant under different temperature conditions A-D: mesophyll cells structure of the twenty-two days old wild type (WT) (A) and tsa2 mutant (B, C, D) seeded under different temperature conditions; E, F, G, H: magnified map of dashed area in A, B, C, D, respectively; I, J: mesophyll cells structure of twenty-two days old tsa2 mutant seeded under 22°C and transferred to 28°C (I) and 32°C (J) for 10 days, respectively; K, L: mesophyll cells structure of tsa2 mutant seeded under 28°C and transferred to 22°C (K) and 32°C (L) for 10 days, respectively; M, N, O, P: magnified map of dashed area in I, J, K, L, respectively. A-D and I-L, Bar=2 μm; E-H and M-P, Bar=500 nm."

Fig. 6

Expression analysis of genes in photosynthetic pigment metabolism, chloroplast development and photosynthesis of the wild type (WT) and tsa2 mutant leaves **: significant difference at P < 0.01 by t-test."

Table 1

Primers of photosynthetic pigment metabolism, chloroplast development and photosynthesis-related genes used for quantitative real-time PCR"

引物
Primer
正向序列
Forward sequence (5'-3')
反向序列
Reverse sequence (5'-3')
UBIQUITIN 5 ACCACTTCGACCGCCACTACT ACGCCTAAGCCTGCTGGTT
OsCAO1 GACACCTTCATCTGGGCTTCAA CGAGAGACATCCGGTAGAGC
OsCHLI GTTCGAGCCTGGTTTGCTTGC CTCTCCACGGTGTTCCATCCTG
OsCHLa/b GGTGGTCAAGGTGTCATTGTCAT ACGCGACTGGATCTTTGGAGAG
OsCHLM CCATCCATTGGTCTCCTTATGACA GTAGCCTACTTACCATCAATGAGTC
OsCHLD GCTTGCAGAAAGCTACACAAGC AGGCCGTGAGCTAAAGGAGA
OsDVR CAGGTCGAGACCGTCAAGAAC ATGACCTGGATCGGCACCTTG
OsHEMD TGGAAGGCTGCTGGAAATCCTAAG TCCTTGGAAGCTCTGAGGCCAA
OsPSY1 GCCTCAAGCAGGCCTATCATC GTGATGTGCGAGGCATTTGGTC
OsPSY2 GACAAATTCTGCGTGCCAGGTT GACAGCAGCTTCTTTGCCTTGTT
OsPSY3 TTCAGACAGGCCGAAGAAGGC GTAGGCCCTCTTGGTGAAGTTGT
OsPSAA TGGGGTTGATCCTAAGGAGATACCA CCTCCGCGAAAACTAAGAAATTCTG
OsPSAB TGGCAGGGCAACGTTTCACAATT CAGTCGCCCAAACAAGATGTCCAAAT
OsPSAC GTGTACGAGCTTGTCCAACAGATGTAT GCAGGCGGATTCGCATCTCTTAC
OsPSAD AGCAGGTGTTCGAGATGCCCAC ATTGGGGAAGACGCGGTAGAACT
OsPSAE AGGCACCAAGGTGAAGATCCTGAG AGGGCGTAGTTGTTGGTCGACAC
OsPSAF TCAAGAAGCTCCAGTCGTCGCTC AGGCCGAACTTGCCGTAGTTCTC
OsPSAH GTCGCCGTACAACCCTCTCCAG CTTCTTGATCGGAAGCAGGTCCG
OsPSAL TCTGAGAAGCCAACGTACCAGGTG AGGTTGGAGAGGTACCAGGCGAC
OsPSBA GCGGTTCCCTATTCAGTGCTATG TAACCATGAGCGGCCACAATATT
OsPSBB TAGTTTCTGGTTGGGCTGGCTC CTCCAACCACCCCACGAATTG
OsPSBD GTAGGATGGTCTGGCCTATTGCTT ACTATTGGCAGGGGTGGAAACTG
OsPSBE TGTCTGGAAGCACGGGAGAACGT GTTTGGCCGAGGACTTCCAAACAC
OsPSBF CTATTTTTACAGTGCGATGGCTGG TATCGTTGGATGAACTGCATTGCT
OsPSBO TCGAGGAGAAGGACGGAATCGAC CTTTGGGTCGAGGAAGGACGAAC
OsPSBY TGCGGTCAGACTGAGAGCTTGAG AAGGGAAGAGAGGATTAGGAACAGGATT
OsPETA GCAGCAAGGTTATGAAAACCCAC AACAGCACCCACATTCAACCCT
OsPETB TTCAGACCTCGCAACCAGACTG AACAAAAGGCAAGGGTTCTTCGA
OsPETC CTCAAGGGTGACCCGACGTACCT AGGGGCAGATGAACTTGTTCTCG
OsPETD GCGTGGCCCAACGATCTTTTAT TCCAGAGGAGTTGCAAACGGAT
OsPETH GTTCTGGGATCCAGGGTAGCAAC ACTGACATGCAGAGCACCTTGTTC
OsATPA TGAATCTCCTGCTCCGGGTATAAT TGCTGTTTTGCCGGTTTGTCT
OsATPB TCGCAATTCTTGGGTTGGATGA CAACATACTTTCCCGGAGAACCG
OsATPG AGGTGGAGCTCCTCTACTCCAAGT TCAGCTTCCCTTCCTTGGTGGT
OsNDHA CGAGCTGCCGCTCAATCTATTAG AGGCTGACGCCAAAGATTCCATC
OsNDHB TAACAGCTACTCTAGGGGGAATGTT CTTGCCCCACCCATGAGTAAAT
OsRBCS2 ACTCCAAGAGCTCGCAGACC GCCTGTAGTTGGCACCCAGA
OsLHCA2 CCTGGTGGTCTGTGGTTTGACC CCTGGAACCAAGCTCCCATGACG
OsLHCA3 GCTCAGGCTCTTCTCTCTGGGAG CTCAGGGACTGCTTGGATGCGA
OsLHCA4 CCCTTCTCCCACCTACCTCAACG TCAACCCGATCTTCGTCAGCACC
OsLHCA5 TCACCTCGACGGCACATTACCT CTGCTTCAAACCACACTGGCAG
OsLHCB1.3 AAGTGAAGTGGGGGACCGTAGC TCTCGTCGCACTAAACCCATCTTC
OsLHCB2.1 CACGATCGAGATGGTGCCAAC CGGCCTGCGGCTTACATTAA
OsLHCB3 GACTTCAAGGAGCCCGTGTGG CCATGAGGACGACCTGGAATCC
OsLHCB4.1 TCTTTCGCGCGCAATTCAAAC TGCAAGTCGCCATTAACCACC
OsLHCB5 GATGAGCTCGCCAAGTGGTACG CTGAGGCCAAAAGGGTCGTAGC

Table 2

Some polymorphic molecular markers on chromosome 5 in rice"

标记
Marker
正向序列
Forward sequence (5'-3')
反向序列
Reverse sequence (5'-3')
RM405 TATGCTTTCTGTCAGCTTCC CTGCTGTGAAAGAGTTGACG
ZTQ43 TGCAGAGACAAGGAAGCGG TCCTGATCGTTGAGCAGGC
S5-20 TCAGGTCTTACGACGGTATGG GGACACACTAGAATCTACGCACG
S5-57 GAAGCTATTAGCCGGGATCG GCCAAGGCAAAGCTCTCTT
S5-119 AGCGCAGATATGCTTTCCAA TATGGCAGTGCAGAGGTGA
RM18053 GAGACCAGAGGGAGACAAAGA CTTAGGTCTCCCGACAGTCACG

Fig. 7

Molecular mapping of TSA2 on chromosome 5 in rice n = 285: number of plant in primary mapping; n = 1150: number of plant in fine mapping."

Table 3

Subcellular localization prediction of protein in TSA2 gene mapping interval"

基因登录号
Accession number
蛋白质亚细胞定位预测
Protein subcellular localization prediction
(https://www.genscript.com/)
基因登录号
Accession number
蛋白质亚细胞定位预测
Protein subcellular localization prediction
(https://www.genscript.com/)
LOC_Os05g09200 chlo: 7, nucl: 3, mito: 3 LOC_Os05g09640 chlo: 10, nucl: 1, cyto: 1, mito: 1
LOC_Os05g09240 chlo: 7, mito: 6 LOC_Os05g09704 chlo: 9.5, chlo_mito: 5.5, vacu: 2, plas: 1
LOC_Os05g09280 E.R.: 4.5, cyto: 4, E.R._plas: 4, plas: 2.5, mito: 2 LOC_Os05g09708 chlo: 8, cyto: 2, nucl: 1, mito: 1, extr: 1
LOC_Os05g09290 chlo: 14 LOC_Os05g09724 chlo: 8, vacu: 2, nucl: 1, plas: 1, extr: 1
LOC_Os05g09370 chlo: 12, nucl: 1 LOC_Os05g09740 chlo: 11, vacu: 2
基因登录号
Accession number
蛋白质亚细胞定位预测
Protein subcellular localization prediction
(https://www.genscript.com/)
基因登录号
Accession number
蛋白质亚细胞定位预测
Protein subcellular localization prediction
(https://www.genscript.com/)
LOC_Os05g09400 chlo: 12, mito: 2 LOC_Os05g10210 chlo: 4, cyto: 2.5, vacu: 2, cyto_nucl: 2, mito: 1
LOC_Os05g09430 chlo: 9, mito: 3, extr: 1 LOC_Os05g10290 chlo: 9, cyto: 2, mito: 1, extr: 1
LOC_Os05g09450 chlo: 7, extr: 3, nucl: 2, cyto: 1 LOC_Os05g10300 chlo: 3, nucl: 3, E.R.: 3, vacu: 2, mito: 1, plas: 1
LOC_Os05g09480 chlo: 10, mito: 2, nucl: 1 LOC_Os05g10330 chlo: 6, cyto: 2, vacu: 2, E.R.: 2, nucl: 1
LOC_Os05g09490 chlo: 9, cyto: 5 LOC_Os05g10350 chlo: 8, cyto: 3, nucl: 1.5, nucl_plas: 1.5
LOC_Os05g09510 chlo: 12, nucl: 1 LOC_Os05g10380 chlo: 12, mito: 2
LOC_Os05g09540 chlo: 9, mito: 4 LOC_Os05g10420 cyto: 7, chlo: 6
LOC_Os05g09550 chlo: 11, nucl: 1, plas: 1 LOC_Os05g10430 chlo: 6, nucl: 5, extr: 1, E.R.: 1
LOC_Os05g09590 chlo: 5, mito: 5, nucl: 4 LOC_Os05g10550 chlo: 6, nucl: 5, cyto: 3

Table 4

Partial annotated genes in TSA2 gene mapping interval"

基因登录号
Accession number
基因注释
Gene annotation
LOC_Os05g09060 collagen alpha-2, putative, expressed
LOC_Os05g09360 glycine-rich protein, putative, expressed
LOC_Os05g09410 histidine-containing phosphotransfer protein 4, putative, expressed
LOC_Os05g09440 malic enzyme
LOC_Os05g09500 cytosolic hexokinase
LOC_Os05g09520 calmodulin binding protein
LOC_Os05g09600 GA11916-PA, putative, expressed
LOC_Os05g09620 SCC3, putative, expressed
LOC_Os05g09630 homeobox domain containing protein, expressed
LOC_Os05g09650 ubiquinone biosynthesis protein CoQ4, putative, expressed
LOC_Os05g09660 HAD superfamily phosphatase, putative, expressed
LOC_Os05g09680 acid phosphatase family, putative, expressed
LOC_Os05g09732 acid phosphatase family, putative, expressed
LOC_Os05g10310 acid phosphatase, putative, expressed
LOC_Os05g10370 acid phosphatase, putative, expressed
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