欢迎访问作物学报，今天是
作物学报

作物学报 ›› 2022, Vol. 48 ›› Issue (7): 1625-1634.doi: 10.3724/SP.J.1006.2022.11043

• 作物遗传育种·种质资源·分子遗传学 • 上一篇    下一篇

长链非编码RNA (LncRNA)在印度梨形孢促进大麦根部生长发育中的调控作用

郭楠楠(), 刘天策, 史硕, 胡心亭, 牛亚丹, 李亮()   

  1. 河北工业大学化工学院, 天津 300130
  • 收稿日期:2021-04-13 接受日期:2021-10-19 出版日期:2022-07-12 网络出版日期:2021-11-02
  • 通讯作者: 李亮
  • 作者简介:E-mail: 15033355861@163.com
  • 基金资助:
    国家自然科学基金项目(31801948);河北省重点研发计划项目(19226505D);河北省自然科学基金项目(C2021202005)

Regulation of long non-coding RNA (LncRNA) in barley roots in response to Piriformospora indica colonization

GUO Nan-Nan(), LIU Tian-Ce, SHI Shuo, HU Xin-Ting, NIU Ya-Dan, LI Liang()   

  1. College of Chemical Engineering and Technology, Hebei University of Technology, Tianjin 300130, China
  • Received:2021-04-13 Accepted:2021-10-19 Published:2022-07-12 Published online:2021-11-02
  • Contact: LI Liang
  • Supported by:
    National Natural Science Foundation of China(31801948);Key Research & Development Projects in Hebei Province(19226505D);Natural Science Foundation of Hebei Province(C2021202005)

RichHTML

16

PDF

135

摘要：

印度梨形孢定殖植物会促进植物生物产量提高, 其分子机制有待深入挖掘。LncRNA是一类长链非编码RNA, 在植物生长发育过程中具有重要调控作用。然而, 目前我们还不清楚大麦中LncRNA是否对印度梨形孢的定殖有响应。本研究发现, 印度梨形孢定殖大麦会诱导大麦根系迅速发育, 促进较多根分枝。采用全基因组高通量测序RNA-seq和生物信息学方法鉴定LncRNA, 发现在P. indica定殖后3 d和7 d分别有752个和932个差异表达的LncRNA, 7 d相对于3 d有70个差异表达的LncRNA。其中在P. indica定殖后3 d有375个LncRNA表达上调, 377个LncRNA表达下调; 在P. indica定殖后7 d有459个LncRNA表达上调, 473个LncRNA表达下调; 7 d相对于3 d组中, 有39个LncRNA表达上调, 31个LncRNA表达下调。qPCR验证LncRNA的表达与RNA-seq结果一致。GO和KEGG分析表明, 在P. indica定殖大麦促生过程中, 部分LncRNA参与了激素信号途径的转录调控。该工作对于进一步理解LncRNA与靶基因的相互作用以及其对靶基因的调控功能提供了新的理论基础和实验依据, 并以LncRNA为靶点, 进行作物性状改良提供新的思路和方向。

关键词: LncRNA, 大麦, 印度梨形孢, RNA-seq, 转录因子, 细胞周期

Abstract:

The molecular mechanism of biomass enhancement by Piriformospora indica in colonization plants needs to be further explored. LncRNA is a kind of long-chain non-coding RNA, which plays an important role in the regulation of plant growth and development. However, it remains unclear whether barley LncRNAs are responsive to Piriformospora indica colonization. It was found that barley roots exhibited fast development and large roots branched after P. indica colonization. Genome-wide high throughput RNA-seq and bioinformatical analysis showed that 752 and 932 differentially expressed LncRNAs were detected in responsive to P. indica at 3-day and 7-day after colonization, respectively. And 70 differentially expressed LncRNAs were found at 7-day compared to 3-day. Among these, 375 were up-regulated and 377 were down-regulated after 3 days’ colonization, and 459 were up-regulated and 473 were down-regulated after 7 days’ colonization, 39 were up-regulated and 31 were down-regulated in 7-day to 3-day comparison group. The qPCR results verified the validity of LncRNAs data in RNA-seq. GO and KEGG analysis indicated that a few LncRNAs might be involved in the molecular functions, cellular components, and biological processes upon P. indica colonization. This study provides a new theoretical basis and experimental basis for further understanding of the interaction between LncRNAs and coding sequences and regulatory functional networks, and provides new ideas and directions for crop shape improvement based on LncRNAs.

Key words: LncRNA, barley, Piriformospora indica, RNA-seq, transcription factor, cell cycle

图1

大麦在P. indica定殖后3 d和7 d形态、根长与根数统计结果图 A: 处理组与对照组在3 d的根长和根数, 标尺为 1.0 cm; B: 处理组与对照组在3 d根的分枝情况, 标尺为1.0 cm; C: 处理组与对照组在3 d和7 d的根长统计; D: 处理组与对照组在3 d和7 d的根数统计。进行3个生物学重复实验和统计分析。"

图2

LncRNA 鉴定的高通量测序流程图"

图3

差异表达的LncRNA的层次聚类热图 横坐标为样本名称, 纵坐标为差异表达的LncRNA, 左侧根据表达相似程度对基因进行聚类, 上方根据表达谱的相似程度对每个样本进行聚类, 由蓝至红表达量逐渐上调, 数字为均一化后的相对表达量。"

图4

差异表达LncRNA火山图 A: 3 d vs Mock比较组中差异表达的LncRNA; B: 7 d vs Mock 比较组中差异表达的LncRNA; C: 7 d vs 3 d比较组中差异表达的LncRNA。横坐标表示基因在不同样本或比较组合间的表达倍数变化(log2 (Fold Change)), 横坐标的绝对值越大表明两个比较组合之间的表达变化倍数越大; 纵坐标表示表达差异的显著性水平。表达上调基因用红色点表示, 下调基因用绿色点表示, 蓝色点为未发生显著变化的基因(Padj < 0.05) 。"

表1

用于LncRNA差异表达鉴定的引物"

基因编号
Gene code		 上游引物序列
Forward sequence (5'-3')		 下游引物序列
Reverse sequence (5'-3')
XLOC-070335 TGGCGTCCATATTACGAGGT TTCGGGGAAATATGCTTTTG
XLOC-318641 CATTAGGGAATCCGACGAGA AGTCACGGTTACGCACACAG
XLOC-067560 CCAGTGCAATGATCGCTAGA GGCCTGCTGTCCTTGTTATC
XLOC-119623 TCCGTTTGGTGATTGTGTGT TGCACACGTACAGGGATGAT
XLOC-322519 AGGTAGGTCTCCGTGGGTCT CGAAACCCTCGTTTTGTGTT
XLOC-206343 TCCCCTCTCGTAGATGGACA GACTAAGGAGGGCAGCAAAA
HvUBIQUITIN ACCCTCGCCGACTACAACAT CAGTAGTGGCGGTCGAAGTG

图5

qRT-PCR鉴定LncRNA的差异表达 A: LncRNA_XLOC_070335、XLOC_318641和XLOC_067560基因表达上调; B: LncRNA_XLOC_119623、XLOC_322519和XLOC_206343基因表达下调。qRT-PCR实验和数据分析进行3个生物学重复。*显著差异(P < 0.05)。"

图6

GO富集柱状图 A: 3 d vs Mock组中GO 的富集; B: 7 d vs Mock组中GO的富集; C: 7 d vs 3 d组中GO的富集; 横坐标表示GO条目名称, 分为3类(BP生物学过程, CC细胞组分, MF分子功能)用不同条框区分, 纵坐标为GO条目富集的基因数。"

图7

3个比较组在KEGG途径中富集的差异表达的LncRNA 图中纵坐标代表不同的通路, 横坐标代表相应通路显著差异表达基因占该通路所有基因的比例。圆圈大小代表富集在相应通路中的基因数目, 圆圈越大, 代表富集在该通路中的基因越多。颜色代表富集显著性, 越接近黑色, 代表越显著。"

图8

植物激素信号转导途径"

[1] Kitagawa M, Kitagawa K, Kotake Y, Niida H, Ohhata T. Cell cycle regulation by long non-coding RNAs. Cell Mol Life Sci, 2013, 70: 4785-4794.
doi: 10.1007/s00018-013-1423-0
[2] Wilusz J E, Sunwoo H, Spector D L. Long noncoding RNAs: functional surprises from the RNA world. Genes Dev, 2009, 23: 1494-1504.
doi: 10.1101/gad.1800909
[3] Rinn J L, Chang H Y. Genome regulation by long noncoding RNAs. Annu Rev Biochem, 2012, 81: 145-166.
doi: 10.1146/annurev-biochem-051410-092902
[4] Kang C, Liu Z. Global identification and analysis of long non-coding RNAs in diploid strawberry Fragaria vesca during flower and fruit development. BMC Genomics, 2015, 16: 815.
doi: 10.1186/s12864-015-2014-2
[5] Li C, Qiao Z, Qi W, Wang Q, Yuan Y, Yang X, Tang Y, Mei B, Lyu Y, Zhao H, Xiao H, Song R. Genome-wide characterization of cis-acting DNA targets reveals the transcriptional regulatory framework of opaque2 in maize. Plant Cell, 2015, 27: 532-545.
doi: 10.1105/tpc.114.134858
[6] Chekanova J A. Long non-coding RNAs and their functions in plants. Curr Opin Plant Biol, 2015, 27: 207-216.
doi: 10.1016/j.pbi.2015.08.003 pmid: 26342908
[7] Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi P P. A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell, 2011, 146: 353-358.
doi: 10.1016/j.cell.2011.07.014
[8] Rubio-Somoza I, Weigel D, Franco-Zorilla J M, Garcia J A, Paz-Ares J. ceRNAs: miRNA target mimic mimics. Cell, 2011, 147: 1431-1432.
doi: 10.1016/j.cell.2011.12.003 pmid: 22196719
[9] Fan C, Hao Z, Yan J, Li G. Genome-wide identification and functional analysis of lincRNAs acting as miRNA targets or decoys in maize. BMC Genomics, 2015, 16: 793.
doi: 10.1186/s12864-015-2024-0
[10] Shuai P, Liang D, Tang S, Zhang Z, Ye C Y, Su Y, Xia X, Yin W.Genome-wide identification and functional prediction of novel and drought-responsive lincRNAs in Populus trichocarpa. J Exp Bot, 2014, 65: 4975-4983.
doi: 10.1093/jxb/eru256 pmid: 24948679
[11] Wang T Z, Liu M, Zhao M G, Chen R, Zhang W H. Identification and characterization of long non-coding RNAs involved in osmotic and salt stress in Medicago truncatula using genome-wide high-throughput sequencing. BMC Plant Biol, 2015, 15: 131.
doi: 10.1186/s12870-015-0530-5
[12] Lu X, Chen X, Mu M, Wang J, Wang X, Wang D, Yin Z, Fan W, Wang S, Guo L, Ye W. Genome-wide analysis of long noncoding RNAs and their responses to drought stress in cotton (Gossypium hirsutum L.). PLoS One, 2016, 11: e0156723.
doi: 10.1371/journal.pone.0156723
[13] Lyu Y, Liang Z, Ge M, Qi W, Zhang T, Lin F, Peng Z, Zhao H. Genome-wide identification and functional prediction of nitrogen-responsive intergenic and intronic long non-coding RNAs in maize (Zea mays L.). BMC Genomics, 2016, 17: 350.
doi: 10.1186/s12864-016-2650-1
[14] Xin M, Wang Y, Yao Y, Song N, Hu Z, Qin D, Xie C, Peng H, Ni Z, Sun Q. Identification and characterization of wheat long non-protein coding RNAs responsive to powdery mildew infection and heat stress by using microarray analysis and SBS sequencing. BMC Plant Biol, 2011, 11: 61.
doi: 10.1186/1471-2229-11-61
[15] Shumayla, Sharma S, Taneja M, Tyagi S, Singh K, Upadhyay S K. Survey of High Throughput RNA-Seq Data reveals potential roles for LncRNAs during development and stress response in bread wheat. Front Plant Sci, 2017, 8: 1019.
doi: 10.3389/fpls.2017.01019 pmid: 28649263
[16] Heo J B, Sung S. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science, 2011, 331: 76-79.
doi: 10.1126/science.1197349
[17] Swiezewski S, Liu F, Magusin A, Dean C. Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature, 2009, 462: 799-802.
doi: 10.1038/nature08618
[18] Ding J, Lu Q, Ouyang Y, Mao H, Zhang P, Yao J, Xu C, Li X, Xiao J, Zhang Q. A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice. Proc Natl Acad Sci USA, 2012, 109: 2654-2659.
doi: 10.1073/pnas.1121374109
[19] Qin T, Zhao H, Cui P, Albesher N, Xiong L. A nucleus-localized long non-coding RNA enhances drought and salt stress tolerance. Plant Physiol, 2017, 175: 1321-1336.
doi: 10.1104/pp.17.00574
[20] Zou Y, Tang H, Li T, Sun M, Qu X, Zhou J, Yang C, Mu Y, Jiang Q, Liu Y, Chen G, Chen G, Zheng Y, Wei Y, Lan X, Ma J. Identification and characterization of mRNAs and LncRNAs of a barley shrunken endosperm mutant using RNA-seq. Genetica, 2020, 148: 55-68.
doi: 10.1007/s10709-020-00087-2
[21] Karlik E, Gözükırmızı N. Evaluation of barley LncRNAs expression analysis in salinity stress. Russ J Genet, 2018, 54: 198-204.
doi: 10.1134/S1022795418020096
[22] Unver T, Tombuloglu H. Barley long non-coding RNAs (LncRNA) responsive to excess boron. Genomics, 2020, 112: 1947-1955.
doi: 10.1016/j.ygeno.2019.11.007
[23] Michael A H, Bryan P, Amanda S B, Sarah A K, Wei Y, Steven R S, Nicholas C C. Small-interfering RNAs from natural antisense transcripts derived from a cellulose synthase gene modulate cell wall biosynthesis in barley. Proc Natl Acad Sci USA, 2008, 105: 20534-20539.
doi: 10.1073/pnas.0809408105
[24] Qiu C W, Zhao J, Chen Q, Wu F. Genome-wide characterization of drought stress responsive long non-coding RNAs in Tibetan wild barley. Environ Exp Bot, 2019, 164: 124-134.
doi: 10.1016/j.envexpbot.2019.05.002
[25] Karlik E, Gozukirmizi N. Expression analysis of LncRNA AK370814 involved in the barley vitamin B6 salvage pathway under salinity. Mol Biol Rep, 2018, 45: 1597-1609.
doi: 10.1007/s11033-018-4289-2 pmid: 30298351
[26] Weiss M, Selosse M A, Rexer K H, Urban A, Oberwinkler F. Sebacinales: a hitherto overlooked cosm of heterobasidiomycetes with a broad mycorrhizal potential. Mycol Res, 2004, 108: 1003-1010.
doi: 10.1017/S0953756204000772
[27] Ghaffari M R, Mirzaei M, Ghabooli M, Khatabi B, Wu Y, Zabet-Moghaddam M, Mohammadi-Nejad G, Haynes P A, Hajirezaei M R, Sepehri M, Salekdeh G H. Root endophytic fungus Piriformospora indica improves drought stress adaptation in barley by metabolic and proteomic reprogramming. Environ Exp Bot, 2019, 157: 197-210.
doi: 10.1016/j.envexpbot.2018.10.002
[28] Sherameti I, Venus Y, Drzewiecki C, Tripathi S, Dan V M, Nitz I, Varma A, Grundler F M, Oelmuller R. PYK10, a b-glucosidase located in the endoplasmatic reticulum, is crucial for the beneficial interaction between Arabidopsis thaliana and the endophytic fungus Piriformospora indica. Plant J, 2008, 54: 428-439.
doi: 10.1111/j.1365-313X.2008.03424.x
[29] Zhang W, Wang J, Xu L, Wang A, Huang L, Du H, Qiu L, Oelmuller R. Drought stress responses in maize are diminished by Piriformospora indica. Plant Signal Behav, 2018, 13: e1414121.
doi: 10.1080/15592324.2017.1414121
[30] Abdelaziz M E, Abdelsattar M, Abdeldaym E A, Atia M A M, Mahmoud A W M, Saad M M, Hirt H. Piriformospora indica alters Na+/K+ homeostasis, antioxidant enzymes and LeNHX1 expression of greenhouse tomato grown under salt stress. Sci Hortic (Amsterdam), 2019, 256: 108532.
doi: 10.1016/j.scienta.2019.05.059
[31] Varma A, Verma S, Sudha X, Sahay N, Butehorn B, Franken P. Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Appl Environ Microbiol, 1999, 65: 2741-2744.
doi: 10.1128/AEM.65.6.2741-2744.1999
[32] Yang L, Cao J L, Zou Y N, Wu Q S, Kuča K. Piriformospora indica: a root endophytic fungus and its roles in plants. Not Bot Hortic Agrobo, 2020, 48: 1-13.
[33] Bagde U S, Prasad R, Varma A. Impact of culture filtrate of Piriformospora indica on biomass and biosynthesis of active ingredient aristolochic acid in Aristolochia elegans Mart. Int J Agric Biol, 2013, 6: 29-37.
[34] Kumar V, Sarma M V, Saharan, Kumar L, Sahai V, Bisaria V S, Sharma A K. Effect of formulated root endophytic fungus Piriformospora indica and plant growth promoting rhizobacteria fluorescent pseudomonads R62 and R81 on Vigna mungo. World J Microbiol Biotechnol, 2012, 28: 595-603.
doi: 10.1007/s11274-011-0852-x
[35] Sharma G, Agrawal V. Marked enhancement in the artemisinin content and biomass productivity in Artemisia annua L. shoots co-cultivated with Piriformospora indica. World J Microbiol Biotechnol, 2013, 29: 1133-1138.
doi: 10.1007/s11274-013-1263-y
[36] Vadassery J, Ranf S, Drzewiecki C, Mithofer A, Mazars C, Scheel D, Lee J, Oelmuller R. A cell wall extract from the endophytic fungus Piriformospora indica promotes growth of Arabidopsis seedlings and induces intracellular calcium elevation in roots. Plant J, 2009, 59: 193-206.
doi: 10.1111/j.1365-313X.2009.03867.x
[37] Yadav V, Kumar M, Deep D K, Kumar H, Sharma R, Tripathi T, Tuteja N, Saxena A K, Johri A K. Withdrawal: a phosphate transporter from the root endophytic fungus Piriformospora indica plays a role in phosphate transport to the host plant. J Biol Chem, 2010, 285: 26532-26544.
doi: 10.1074/jbc.M110.111021
[38] Lee Y C, Johnson J M, Chien C T, Sun C, Cai D, Lou B, Oelmüller R, Yeh K W. Growth promotion of Chinese cabbage and Arabidopsis by Piriformospora indica is not stimulated by Mycelium-synthesized auxin. Mol Plant Microbe Interact, 2011, 24: 421-443.
doi: 10.1094/MPMI-05-10-0110
[39] Sun C, Johnson J M, Cai D, Sherameti I, Oelmuller R, Lou B. Piriformospora indica confers drought tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of drought-related genes and the plastid-localized CAS protein. J Plant Physiol, 2010, 167: 1009-1017.
doi: 10.1016/j.jplph.2010.02.013
[40] Baltruschat H, Fodor J, Harrach B D, Niemczyk E, Barna B, Gullner G, Janeczko A, Kogel K H, Schafer P, Schwarczinger I, Zuccaro A, Skoczowski A. Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol, 2008, 180: 501-510.
doi: 10.1111/j.1469-8137.2008.02583.x pmid: 18681935
[41] Schafer P, Pfiffi S, Voll L M, Zajic D, Chandler P M, Waller F, Scholz U, Pons-Kuhnemann J, Sonnewald S, Sonnewald U, Kogel K H.Manipulation of plant innate immunity and gibberellin as factor of compatibility in the mutualistic association of barley roots with Piriformospora indica. Plant J, 2009, 59: 461-474.
doi: 10.1111/j.1365-313X.2009.03887.x
[42] Zuccaro A, Lahrmann U, Guldener U, Langen G, Pfiffi S, Biedenkopf D, Wong P, Samans B, Grimm C, Basiewicz M, Murat C, Martin F, Kogel K H.Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathog, 2011, 7: e1002290.
doi: 10.1371/journal.ppat.1002290
[1] 李佩婷, 赵振丽, 黄潮华, 黄国强, 徐良年, 邓祖湖, 张玉, 赵新旺. 基于转录组及WGCNA的甘蔗干旱响应调控网络分析[J]. 作物学报, 2022, 48(7): 1583-1600.
[2] 韩尚玲, 霍轶琼, 李辉, 韩华蕊, 侯思宇, 孙朝霞, 韩渊怀, 李红英. 基于WGCNA发掘谷子穗部类黄酮合成途径调控关键基因[J]. 作物学报, 2022, 48(7): 1645-1657.
[3] 柯丹霞, 霍娅娅, 刘怡, 李锦颖, 刘晓雪. 大豆TGA转录因子基因GmTGA26在盐胁迫中的功能分析[J]. 作物学报, 2022, 48(7): 1697-1708.
[4] 田甜, 陈丽娟, 何华勤. 基于Meta-QTL和RNA-seq的整合分析挖掘水稻抗稻瘟病候选基因[J]. 作物学报, 2022, 48(6): 1372-1388.
[5] 李阿立, 冯雅楠, 李萍, 张东升, 宗毓铮, 林文, 郝兴宇. 大豆叶片响应CO2浓度升高、干旱及其交互作用的转录组分析[J]. 作物学报, 2022, 48(5): 1103-1118.
[6] 朱峥, 王田幸子, 陈悦, 刘玉晴, 燕高伟, 徐珊, 马金姣, 窦世娟, 李莉云, 刘国振. 水稻转录因子WRKY68在Xa21介导的抗白叶枯病反应中发挥正调控作用[J]. 作物学报, 2022, 48(5): 1129-1140.
[7] 陈悦, 孙明哲, 贾博为, 冷月, 孙晓丽. 水稻AP2/ERF转录因子参与逆境胁迫应答的分子机制研究进展[J]. 作物学报, 2022, 48(4): 781-790.
[8] 赵改会, 李书宇, 詹杰鹏, 李晏斌, 师家勤, 王新发, 王汉中. 甘蓝型油菜角果数突变体基因的定位及候选基因分析[J]. 作物学报, 2022, 48(1): 27-39.
[9] 王娜, 白建芳, 马有志, 郭昊宇, 王永波, 陈兆波, 赵昌平, 张立平. 小麦lncRNA27195及其靶基因TaRTS克隆及表达分析[J]. 作物学报, 2021, 47(8): 1417-1426.
[10] 曾维英, 赖振光, 孙祖东, 杨守臻, 陈怀珠, 唐向民. 基于BSA-Seq和RNA-Seq方法鉴定大豆抗豆卷叶螟候选基因[J]. 作物学报, 2021, 47(8): 1460-1471.
[11] 贺军与, 钟伟, 陈云琼, 王卫斌, 熊静蕾, 蒋亚丽, 施辉蒙, 陈升位. 大麦籽粒发育进程中7种黄酮类化合物的积累特性分析[J]. 作物学报, 2021, 47(8): 1624-1630.
[12] 耿腊, 黄业昌, 李梦迪, 谢尚耿, 叶玲珍, 张国平. 大麦籽粒β-葡聚糖含量的全基因组关联分析[J]. 作物学报, 2021, 47(7): 1205-1214.
[13] 尹明, 杨大为, 唐慧娟, 潘根, 李德芳, 赵立宁, 黄思齐. 大麻GRAS转录因子家族的全基因组鉴定及镉胁迫下表达分析[J]. 作物学报, 2021, 47(6): 1054-1069.
[14] 葛敏, 王元琮, 宁丽华, 胡梦梅, 石习, 赵涵. 氮响应转录因子ZmNLP5影响玉米根系生长的功能研究[J]. 作物学报, 2021, 47(5): 807-813.
[15] 张帆, 杨茜. 大麦-双季稻轮作体系有机物料与化肥配施对大麦资源利用效率及产量的影响[J]. 作物学报, 2021, 47(12): 2522-2531.
Viewed
Full text


Abstract

Cited
  Shared   
  Discussed   
[1] 李绍清, 李阳生, 吴福顺, 廖江林, 李达模. 水稻孕穗期在淹涝胁迫下施肥的优化选择及其作用机理[J]. 作物学报, 2002, 28(01): 115 -120 .
[2] 王兰珍;米国华;陈范骏;张福锁. 不同产量结构小麦品种对缺磷反应的分析[J]. 作物学报, 2003, 29(06): 867 -870 .
[3] 杨建昌;张亚洁;张建华;王志琴;朱庆森. 水分胁迫下水稻剑叶中多胺含量的变化及其与抗旱性的关系[J]. 作物学报, 2004, 30(11): 1069 -1075 .
[4] 袁美;杨光圣;傅廷栋;严红艳. 甘蓝型油菜生态型细胞质雄性不育两用系的研究Ⅲ. 8-8112AB的温度敏感性及其遗传[J]. 作物学报, 2003, 29(03): 330 -335 .
[5] 王永胜;王景;段静雅;王金发;刘良式. 水稻极度分蘖突变体的分离和遗传学初步研究[J]. 作物学报, 2002, 28(02): 235 -239 .
[6] 王丽燕;赵可夫. 玉米幼苗对盐胁迫的生理响应[J]. 作物学报, 2005, 31(02): 264 -268 .
[7] 田孟良;黄玉碧;谭功燮;刘永建;荣廷昭. 西南糯玉米地方品种waxy基因序列多态性分析[J]. 作物学报, 2008, 34(05): 729 -736 .
[8] 胡希远;李建平;宋喜芳. 空间统计分析在作物育种品系选择中的效果[J]. 作物学报, 2008, 34(03): 412 -417 .
[9] 王艳;邱立明;谢文娟;黄薇;叶锋;张富春;马纪. 昆虫抗冻蛋白基因转化烟草的抗寒性[J]. 作物学报, 2008, 34(03): 397 -402 .
[10] 郑希;吴建国;楼向阳;徐海明;石春海. 不同环境条件下稻米组氨酸和精氨酸的胚乳和母体植株QTL分析[J]. 作物学报, 2008, 34(03): 369 -375 .
京ICP备15008789号-2