Welcome to Acta Agronomica Sinica，

Acta Agron Sin ›› 2017, Vol. 43 ›› Issue (10): 1480-1488.doi: 10.3724/SP.J.1006.2017.01480

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

Evolutionary Fate and Expression Pattern of Genes Related to Proline Biosynthesis in Brassica napus

WANG Cui-Ping1,HUA Xue-Jun2,LIN Bin3,LIU Ai-Hua4   

  1. 1 State Key Laboratory of Seedling Bioengineering, Ningxia Forestry Institute, Yinchuan 750004, China; 2 Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China; 3 University of Chinese Academy of Sciences, Beijing 100049, China; 4 Department of Plant Science, University of Manitoba, Winnipeg, R3T2N2, MB, Canada
  • Received:2017-01-17 Revised:2017-05-10 Online:2017-10-12 Published:2017-05-22
  • Contact: Hua Xuejun, E-mail: xjhua@ibcas.ac.cn E-mail:wangcuipingcas@163.com
  • Supported by:

    The study was supported by the Ningxia Natural Science Foundation of China (NZ16215).

RichHTML

PDF

863

Abstract:

Proline accumulation is a widespread metabolic adaptation in many organisms in response to various environmental stresses, and it was proved to play protective roles for plants under adverse conditions. Polyploidization is a prominent driving force during plant evolution and many important crops have experienced this process during their evolutionary history. Brassica napus (AACC) is believed to be a newly formed allotetraploid, evolving from the inter‐specific hybridization of two diploids, B. rapa (AA) and B. oleracea (CC) followed by chromosome doubling. In this research, we studied the evolutionary fate of genes related to proline synthesis in allotetraploid (B. napus), and its diploids ancestors (B. rapa and B. oleracea), to explore the effect of polyploidition on homologous gene evolution. First, we obtained the genes for proline biosynthesis (P5CSs, OAT) by database searching, and studied the similarities and the expression regulation pattern of homologous genes in allotetraploid (B. napus), in comparison with its diploids progenitors (B. rapa and B. oleracea), in different organs and in response to salt stress. Sequence analysis and phylogenetic analysis revealed that BnaA.P5CS2.a, BnaA.P5CS2.b and BnaC.P5CS2.c originated from BraA.P5CS2.a, BraA.P5CS2.b, and BolC.P5CS2.a, respectively; BnaA.OAT.a, BnaC.OAT.b originated from BraA.OAT.a and BolC.OAT.a, respectively. And, one copy of gene loss from B. oleracea occurred for BnP5CS2 but not for BnOAT. Expression patterns of these homologous genes in response to salt stress in different organs were also characterized by semi-quantitive RT-PCR. In B. napus, two homologous gene pairs with different origins, BnaA.P5CS2.a and BnaC.P5CS2.c, BnaA.OAT.a and BnaC.OAT.b exhibited biased expression in different organs, implying possible sub-functionalization of P5CS2 and OAT. The genes BnaA.P5CS1.a and BnaC.P5CS1.d with different diploid ancestors were induced by NaCl treatment, and the expression of BnaC.P5CS1.d was higher than that of BnaA.P5CS1.a, showing a biased expression. RT-PCR manifested that preservation of expression pattern of original genes in diploid was found for P5CS1 (BnaA.P5CS1.a and BnaC.P5CS1.d), P5CS2 (BnaA.P5CS2.a and BnaC.P5CS2.c). These results suggest that the gene sequence and expression pattern existing in allotetraploid (B. napus) were conserved, which is benefit to proline accumulation for plant adaptation to environmental stresses.

Key words: Polyploidization, Proline biosynthesis, Biased expression, Salt stress, Sub-functionalization

[1] Kishor P B K, Hong Z L, Miao G H, Hu C A A, Verma D P S. Overexpression of Δ1-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol, 1995, 108: 1387–1394 [2] Schat H, Sharma S S, Vooijs R. Heavy metal-induced accumulation of free proline in a metal-tolerant and a nontolerant ecotype of Silene vulgaris. Physiol Plantarum, 1997, 101: 477–482 [3] Yang S L, Lan S S, Gong M. Hydrogen peroxide-induced proline and metabolic pathway of its accumulation in maize seedlings. J Plant Physiol, 2009, 166: 1694–1699 [4] Tavakoli M, Poustini K, Alizadeh H. Proline accumulation and related genes in wheat leaves under salinity stress. J Agric Sci Tech, 2016, 18: 707–716 [5] Dar M I, Naikoo M I, Rehman F, Naushin F, Khan F A. Proline accumulation in plants: roles in stress tolerance and plant development. In: Iqbal N, Nazar R, Khan N A, eds. Osmolytes and Plants Acclimation to Changing Environment: Emerging Omics Technologies. New Delhi: Springer India Press, 2016. pp 155–166 [6] Chaves M M, Flexas J, Pinheiro C. Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot, 2009, 103: 551–560 [7] Wu H H, Zou Y N, Rahman M M, Ni Q D, Wu Q S. Mycorrhizas alter sucrose and proline metabolism in trifoliate orange exposed to drought stress. Sci Rep, 2017, 7: 42389 [8] Mattioli R, Marchese D, D'Angeli S, Altamura M M, Costantino P, Trovato M. Modulation of intracellular proline levels affects flowering time and inflorescence architecture in Arabidopsis. Plant Mol Biol, 2008, 66: 277–288 [9] Mattioli R, Costantino P, Trovato M. Proline accumulation in plants: not only stress. Plant Signal Behav, 2009, 4: 1016–1018 [10] Mattioli R, Falasca G, Sabatini S, Altamura M M, Costantino P, Trovato M. The proline biosynthetic genes P5CS1 and P5CS2 play overlapping roles in Arabidopsis flower transition but not in embryo development. Physiol Plantarum, 2009, 137: 72–85 [11] Funck D, Winter G, Baumgarten L, Forlani G. Requirement of proline synthesis during Arabidopsis reproductive development. BMC Plant Biology, 2012, 12: 191 [12] Delauney A J, Hu C A A, Kishor P B K, Verma D P S. Cloning of ornithine delta-aminotransferase cDNA from Vigna-Aconitifolia by transcomplementation in Escherichia coli and regulation of proline biosynthesis. J Biol Chem, 1993, 268: 18673–18678 [13] Kishor P B K, Sangam S, Amrutha R N, Laxmi P S, Naidu K R, Rao K R S S, Rao S, Reddy K J, Theriappan P, Sreenivasulu N. Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci India, 2005, 88: 424–438 [14] Wang L, Guo Z, Zhang Y, Wang Y, Yang G, Yang L, Wang R, Xie Z. Characterization of LhSorP5CS, a gene catalyzing proline synthesis in Oriental hybrid lily sorbonne: molecular modelling and expression analysis. Bot Stud, 2017, 58(1): 10 [15] Yoshiba Y, Kiyosue T, Katagiri T, Ueda H, Mizoguchi T, Yamaguchishinozaki K, Wada K, Harada Y, Shinozaki K. Correlation between the induction of a gene for Δ1-pyrroline-5-carboxylate synthetase and the accumulation of proline in Arabidopsis thaliana under osmotic-stress. Plant J, 1995, 7: 751–760 [16] Fabro G, Kovacs I, Pavet V, Szabados L, Alvarez M E. Proline accumulation and AtP5CS2 gene activation are induced by plant-pathogen incompatible interactions in Arabidopsis. Mol Plant Microbe In, 2004, 17: 343–350 [17] Soltis P S, Soltis D E. The role of genetic and genomic attributes in the success of polyploids. Proc Nati Acad Sci USA, 2000, 97: 7051–7057 [18] Buggs R J, Doust A N, Tate J A, Koh J, Soltis K, Feltus F A, Paterson A H, Soltis P S, Soltis D E. Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids. Heredity, 2009, 103: 73–81 [19] Wang J, Tian L, Lee H S, Chen Z J. Nonadditive regulation of FRI and FLC loci mediates flowering-time variation in Arabidopsis allopolyploids. Genetics, 2006, 173: 965–974 [20] Zhao J W, Buchwaldt L, Rimmer S R, Brkic M, Bekkaoui D, Hegedus D. Differential expression of duplicated peroxidase genes in the allotetraploid Brassica napus. Plant Physiol Bioch, 2009, 47: 653–656 [21] Nagahara U. Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilisation. J Jap Bon, 1935, 7: 389–452 [22] Blanc G, Wolfe K H. Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell, 2004, 16: 1679–1691 [23] Yang Y W, Lai K N, Tai P Y, Li W H. Rates of nucleotide substitution in angiosperm mitochondrial DNA sequences and dates of divergence between Brassica and other angiosperm lineages. J Mol Evol, 1999, 48: 597–604 [24] Park J Y, Koo D H, Hong C P, Lee S J, Jeon J W, Lee S H, Yun P Y, Park B S, Kim H R, Bang J W, Plaha P, Bancroft I, Lim Y P. Physical mapping and microsynteny of Brassica rapa ssp. pekinensis genome corresponding to a 222 kbp gene-rich region of Arabidopsis chromosome 4 and partially duplicated on chromosome 5. Mol Genet Genomics, 2005, 274: 579–588 [25] Wang X, Wang H, Wang J, Sun R, Wu J, Liu S, Bai Y, Mun J H, Bancroft I, Cheng F, Huang S, Li X, Hua W, Freeling M, Pires J C, Paterson A H, Chalhoub B, Wang B, Hayward A, Sharpe A G, Park B S, Weisshaar B, Liu B, Li B, Tong C, Song C, Duran C, Peng C, Geng C, Koh C, Lin C, Edwards D, Mu D, Shen D, Soumpourou E, Li F, Fraser F, Conant G, Lassalle G, King G J, Bonnema G, Tang H, Belcram H, Zhou H, Hirakawa H, Abe H, Guo H, Jin H, Parkin I A, Batley J, Kim J S, Just J, Li J, Xu J, Deng J, Kim J A, Yu J, Meng J, Min J, Poulain J, Hatakeyama K, Wu K, Wang L, Fang L, Trick M, Links M G, Zhao M, Jin M, Ramchiary N, Drou N, Berkman P J, Cai Q, Huang Q, Li R, Tabata S, Cheng S, Zhang S, Sato S, Sun S, Kwon S J, Choi S R, Lee T H, Fan W, Zhao X, Tan X, Xu X, Wang Y, Qiu Y, Yin Y, Li Y, Du Y, Liao Y, Lim Y, Narusaka Y, Wang Z, Li Z, Xiong Z, Zhang Z. The genome of the mesopolyploid crop species Brassica rapa. Nat Genet, 2011, 43: 1035–1039 [26] Udall J A, Wendel J F. Polyploidy and crop improvement. Crop Sci, 2006, 46: S3–S14 [27] Wang C P, Lin B, Zhang Y Q, Lin Y H, Liu A H, Hua X J. The evolutionary fate of Δ1-pyrroline-5-carboxylate synthetase 1 (P5CS1) genes in allotetraploid Brassica napus. J Syst Evol, 2014, 52: 566–579 [28] Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol, 2007, 24: 1596–1599 [29] Hua X J, van de Cotte B, Van Montagu M, Verbruggen N. The 5 ' untranslated region of the At-P5R gene is involved in both transcriptional and post-transcriptional regulation. Plant J, 2001, 26: 157–169 [30] ?stergaard L, King G J. Standardized gene nomenclature for the Brassica genus. Plant Methods, 2008, 4: 10 [31] Hua S, Shamsi I H, Guo Y, Pak H, Chen M, Shi C, Meng H, Jiang L. Sequence, expression divergence, and complementation of homologous ALCATRAZ loci in Brassica napus. Planta, 2009, 230: 493–503 [32] Cardenas P D, Gajardo H A, Huebert T, Parkin I A, Iniguez-Luy F L, Federico M L. Retention of triplicated phytoene synthase (PSY) genes in Brassica napus L. and its diploid progenitors during the evolution of the Brassiceae. Theor Appl Genet, 2012, 124: 1215–1228 [33] Deng W, Zhou L, Zhou Y T, Wang Y J, Wang M L, Zhao Y. Isolation and characterization of three duplicated PISTILLATA genes in Brassica napus. Mol Biol Rep, 2011, 38: 3113–3120 [34] Force A, Lynch M, Pickett F B, Amores A, Yan Y L, Postlethwait J. Preservation of duplicate genes by complementary, degenerative mutations. Genetics, 1999, 151: 1531–1545 [35] Adams K L, Liu Z L. Expression partitioning between genes duplicated by polyploidy under abiotic stress and during organ development. Curr Biol, 2007, 17: 1669–1674
[1] YAN Jia-Qian, GU Yi-Biao, XUE Zhang-Yi, ZHOU Tian-Yang, GE Qian-Qian, ZHANG Hao, LIU Li-Jun, WANG Zhi-Qin, GU Jun-Fei, YANG Jian-Chang, ZHOU Zhen-Ling, XU Da-Yong. Different responses of rice cultivars to salt stress and the underlying mechanisms [J]. Acta Agronomica Sinica, 2022, 48(6): 1463-1475.
[2] LEI Xin-Hui, WAN Chen-Xi, TAO Jin-Cai, LENG Jia-Jun, WU Yi-Xin, WANG Jia-Le, WANG Peng-Ke, YANG Qing-Hua, FENG Bai-Li, GAO Jin-Feng. Effects of soaking seeds with MT and EBR on germination and seedling growth in buckwheat under salt stress [J]. Acta Agronomica Sinica, 2022, 48(5): 1210-1221.
[3] DAI Liang-Xiang, XU Yang, ZHANG Guan-Chu, SHI Xiao-Long, QIN Fei-Fei, DING Hong, ZHANG Zhi-Meng. Response of rhizosphere bacterial community diversity to salt stress in peanut [J]. Acta Agronomica Sinica, 2021, 47(8): 1581-1592.
[4] LIU Ya-Wen, ZHANG Hong-Yan, CAO Dan, LI Lan-Zhi. Prediction of drought and salt stress-related genes in rice based on multi-platform gene expression data [J]. Acta Agronomica Sinica, 2021, 47(12): 2423-2439.
[5] Hui LI, De-Fang LI, Yong DENG, Gen PAN, An-Guo CHEN, Li-Ning ZHAO, Hui-Juan TANG. Cloning of the key enzyme gene HcTPPJ in trehalose biosynthesis of kenaf and its expression in response to abiotic stress in kenaf [J]. Acta Agronomica Sinica, 2020, 46(12): 1914-1922.
[6] LI Run-Zhi, JIN Qing, LI Zhao-Hu, WANG Ye, PENG Zhen, DUAN Liu-Sheng. Salicylic acid improved salinity tolerance of Glycyrrhiza uralensis Fisch during seed germination and seedling growth stages [J]. Acta Agronomica Sinica, 2020, 46(11): 1810-1816.
[7] CHEN Xiao-Jing,LIU Jing-Hui,YANG Yan-Ming,ZHAO Zhou,XU Zhong-Shan,HAI Xia,HAN Yu-Ting. Effects of salt stress on physiological indexes and differential proteomics of oat leaf [J]. Acta Agronomica Sinica, 2019, 45(9): 1431-1439.
[8] LI Xu-Kai,LI Ren-Jian,ZHANG Bao-Jun. Identification of rice stress-related gene co-expression modules by WGCNA [J]. Acta Agronomica Sinica, 2019, 45(9): 1349-1364.
[9] TIAN Wen-Gang,ZHU Xue-Feng,SONG Wen,CHENG Wen-Han,XUE Fei,ZHU Hua-Guo. Ectopic expression of S-adenosylmethionine decarboxylase (GhSAMDC1) in cotton enhances salt tolerance in Arabidopsis thaliana [J]. Acta Agronomica Sinica, 2019, 45(7): 1017-1028.
[10] Hua-Ying MAO,Feng LIU,Wei-Hua SU,Ning HUANG,Hui LING,Xu ZHANG,Wen-Ju WANG,Cong-Na LI,Han-Chen TANG,Ya-Chun SU,You-Xiong QUE. A Sugarcane Phosphatidylinositol Transfer Protein Gene ScSEC14 Responds to Drought and Salt Stresses [J]. Acta Agronomica Sinica, 2018, 44(6): 824-835.
[11] Guang-Long ZHU,Cheng-Yu SONG,Lin-Lin YU,Xu-Bing CHEN,Wen-Fang ZHI,Jia-Wei LIU,Xiu-Rong JIAO,Gui-Sheng ZHOU. Alleviation Effects of Exogenous Growth Regulators on Seed Germination of Sweet Sorghum under Salt Stress and Its Physiological Basis [J]. Acta Agronomica Sinica, 2018, 44(11): 1713-1724.
[12] SHA Han-Jing, HU Wen-Cheng, JIA Yan, WANG Xin-Peng, TIAN Xue-Fei, YU Mei-Fang, and ZHAO Hong-Wei*. Effect of Exogenous Salicylic Acid, Proline and γ-Aminobutyric Acid on Yield of Rice under Salt Stress [J]. Acta Agron Sin, 2017, 43(11): 1677-1688.
[13] HOU Lin-Tao,WANG Teng-Yue,JIAN Hong-Ju,WANG Jia,LI Jia-Na,LIU Lie-Zhao. QTL Mapping for Seedling Dry Weight and Fresh Weight under Salt Stress and Candidate Genes Analysis in Brassica napus L. [J]. Acta Agron Sin, 2017, 43(02): 179-189.
[14] HUANGSuo,HULi-Qin,XUDong-Bei,LIWei-Wei,XUZhao-Shi,LILian-Cheng,ZHOUYong-Bin,DIAOXian-Min,JIAGuan-Qing,MAYou-Zhi,CHENMing. Transcription Factor SiNF-YA5 from Foxtail Millet (Setaria italica) Conferred Tolerance to High-salt Stress through ABA-independent Pathway in Transgenic Arabidopsis [J]. Acta Agron Sin, 2016, 42(12): 1787-1797.
[15] QIN Peng-Fei,SHANG Xiao-Guang,SONG Jian,GUO Wang-Zhen. Genome-wide Identification of Acyl-CoA-Binding Protein (ACBP) Gene Family and Their Functional Analysis in Abiotic Stress Tolerance in Cotton [J]. Acta Agron Sin, 2016, 42(11): 1577-1591.
Viewed
Full text


Abstract

Cited
  Shared   
  Discussed   
No Suggested Reading articles found!
Add: No. 80 Xueyuan South Rd, Beijing 100081, P. R. China E-mail: zwxb301@caas.cn
Supported by Beijing Magtech Co.Ltd