Please wait a minute...
Journal of Integrative Agriculture  2020, Vol. 19 Issue (7): 1704-1720    DOI: 10.1016/S2095-3119(19)62761-9
Special Issue: 麦类遗传育种合辑Triticeae Crops Genetics · Breeding · Germplasm Resources
Crop Science Advanced Online Publication | Current Issue | Archive | Adv Search |
Genome-wide identification and transcriptome profiling reveal great expansion of SWEET gene family and their wide-spread responses to abiotic stress in wheat (Triticum aestivum L.)
QIN Jin-xia1, JIANG Yu-jie1, LU Yun-ze1, 3, ZHAO Peng1, WU Bing-jin1, LI Hong-xia1, WANG Yu1, XU Sheng-bao1, SUN Qi-xin2, LIU Zhen-shan1
1 State Key Laboratory of Crop Stress Biology for Arid Areas, College of Agronomy, Northwest A&F University, Yangling 712100, P.R.China
2 Department of Plant Genetics & Breeding, China Agricultural University, Beijing 100193, P.R.China
3 College of Landscape and Ecological Engineering, Hebei University of Engineering, Handan 056021, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
Abstract  
The Sugars Will Eventually be Exported Transporter (SWEET) gene family, identified as sugar transporters, has been demonstrated to play key roles in phloem loading, grain filling, pollen nutrition, and plant-pathogen interactions.  To date, the study of SWEET genes in response to abiotic stress is very limited.  In this study, we performed a genome-wide identification of the SWEET gene family in wheat and examined their expression profiles under mutiple abiotic stresses.  We identified a total of 105 wheat SWEET genes, and phylogenic analysis revealed that they fall into five clades, with clade V specific to wheat and its closely related species.  Of the 105 wheat SWEET genes, 59% exhibited significant expression changes after stress treatments, including drought, heat, heat combined with drought, and salt stresses, and more up-regulated genes were found in response to drought and salt stresses.  Further hierarchical clustering analysis revealed that SWEET genes exhibited differential expression patterns in response to different stress treatments or in different wheat cultivars.  Moreover, different phylogenetic clades also showed distinct response to abiotic stress treatments.  Finally, we found that homoeologous SWEET genes from different wheat subgenomes exhibited differential expression patterns in response to different abiotic stress treatments.  The genome-wide analysis revealed the great expansion of SWEET gene family in wheat and their wide participation in abiotic stress response.  The expression partitioning of SWEET homoeologs under abiotic stress conditions may confer greater flexibility for hexaploid wheat to adapt to ever changing environments.
Keywords:  wheat        sugar transporter        abiotic stress        homoeologous gene        expression partitioning  
Received: 13 March 2019   Accepted:
Fund: This work was supported by the National Natural Science Foundation of China (31601304 and 31601305), the Shaanxi Natural Science Foundation, China (2017JQ3023) and the Doctoral Scientific Research Foundation of Northwest A&F University, China (Z109021611 and Z109021612).
Corresponding Authors:  Correspondence LIU Zhen-shan, E-mail: zhenshanliu@nwafu.edu.cn   
About author:  QIN Jin-xia, E-mail: jinxiaqin2015@nwafu.edu.cn;

Cite this article: 

QIN Jin-xia, JIANG Yu-jie, LU Yun-ze, ZHAO Peng, WU Bing-jin, LI Hong-xia, WANG Yu, XU Sheng-bao, SUN Qi-xin, LIU Zhen-shan. 2020. Genome-wide identification and transcriptome profiling reveal great expansion of SWEET gene family and their wide-spread responses to abiotic stress in wheat (Triticum aestivum L.). Journal of Integrative Agriculture, 19(7): 1704-1720.

Adams K L, Wendel J F. 2005. Polyploidy and genome evolution in plants. Current Opinion in Plant Biology, 8, 135–141.
Almodares A, Hadi M R, Ahmadpour H. 2008. Sorghum stem yield and soluble carbohydrates under different salinity levels. African Journal Biotechnology, 7, 4051–4055.
Anders S, Pyl P T, Huber W. 2015. HTSeq - A Python framework to work with high-throughput sequencing data. Bioinformatics, 31, 166–169.
Chandran D. 2015. Co-option of developmentally regulated plant SWEET transporters for pathogen nutrition and abiotic stress tolerance. IUBMB Life, 67, 461–471.
Chardon F, Bedu M, Calenge F, Klemens P A W, Spinner L, Clement G, Chietera G, Leran S, Ferrand M, Lacombe B, Loudet O, Dinant S, Bellini C, Neuhaus H E, Daniel-Vedele F, Krapp A. 2013. Leaf fructose content is controlled by the vacuolar transporter SWEET17 in Arabidopsis. Current Biology, 23, 697–702.
Chen L Q, Hou B H, Lalonde S, Takanaga H, Hartung M L, Qu X Q, Guo W J, Kim J G, Underwood W, Chaudhuri B, Chermak D, Antony G, White F F, Somerville S C, Mudgett M B, Frommer W B. 2010. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature, 468, 527–534.
Chen L Q, Lin I W N, Qu X Q, Sosso D, McFarlane H E, Londono A, Samuels A L, Frommer W B. 2015. A cascade of sequentially expressed sucrose transporters in the seed coat and endosperm provides nutrition for the Arabidopsis embryo. The Plant Cell, 27, 607–619.
Chen L Q, Qu X Q, Hou B H, Sosso D, Osorio S, Fernie A R, Frommer W B. 2012. Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science, 335, 207–211.
Cheng W H, Endo A, Zhou L, Penney J, Chen H C, Arroyo A, Leon P, Nambara E, Asami T, Seo M, Koshiba T, Sheen J. 2002. A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. The Plant Cell, 14, 2723–2743.
Clavijo B J, Venturini L, Schudoma C, Accinelli G G, Kaithakottil G, Wright J, Borrill P, Kettleborough G, Heavens D, Chapman H, Lipscombe J, Barker T, Lu F H, McKenzie N, Raats D, Ramirez-Gonzalez R H, Coince A, Peel N, Percival-Alwyn L, Duncan O, et?al. 2017. An improved assembly and annotation of the allohexaploid wheat genome identifies complete families of agronomic genes and provides genomic evidence for chromosomal translocations. Genome Research, 27, 885–896.
Dubcovsky J, Dvorak J. 2007. Genome plasticity a key factor in the success of polyploid wheat under domestication. Science, 316, 1862–1866.
Durand M, Porcheron B, Hennion N, Maurousset L, Lemoine R, Pourtau N. 2016. Water deficit enhances C export to the roots in Arabidopsis thaliana plants with contribution of sucrose transporters in both shoot and roots. Plant Physiology, 170, 1460–1479.
Eom J S, Chen L Q, Sosso D, Julius B T, Lin I W, Qu X Q, Braun D M, Frommer W B. 2015. SWEETs, transporters for intracellular and intercellular sugar translocation. Current Opinion in Plant Biology, 25, 53–62.
Feldman M, Levy A A, Fahima T, Korol A. 2012. Genomic asymmetry in allopolyploid plants: Wheat as a model. Journal of Experimental Botany, 63, 5045–5059.
Feng C Y, Han J X, Han X X, Jiang J. 2015. Genome-wide identification, phylogeny, and expression analysis of the SWEET gene family in tomato. Gene, 573, 261–272.
Gao Y, Wang Z Y, Kumar V, Xu X F, Yuan D P, Zhu X F, Li T Y, Jia B L, Xuan Y H. 2018a. Genome-wide identification of the SWEET gene family in wheat. Gene, 642, 284–292.
Gao Y, Zhang C, Han X, Wang Z Y, Ma L, Yuan D P, Wu J N, Zhu X F, Liu J M, Li D P, Hu Y B, Xuan Y H. 2018b. Inhibition of OsSWEET11 function in mesophyll cells improves resistance of rice to sheath blight disease. Molecular Plant Pathology, 19, 2149–2161.
Gaut B S. 2002. Evolutionary dynamics of grass genomes. New Phytologist, 154, 15–28.
Griffiths C A, Paul M J, Foyer C H. 2016. Metabolite transport and associated sugar signalling systems underpinning source/sink interactions. Biochimica et Biophysica Acta-Bioenergetics, 1857, 1715–1725.
Guo W J, Nagy R, Chen H Y, Pfrunder S, Yu Y C, Santelia D, Frommer W B, Martinoia E. 2014. SWEET17, a facilitative transporter, mediates fructose transport across the tonoplast of Arabidopsis roots and leaves. Plant Physiology, 164, 777–789.
Hutin M, Sabot F, Ghesquiere A, Koebnik R, Szurek B. 2015. A knowledge-based molecular screen uncovers a broad-spectrum OsSWEET14 resistance allele to bacterial blight from wild rice. The Plant Journal, 84, 694–703.
Jian H J, Lu K, Yang B, Wang T Y, Zhang L, Zhang A X, Wang J, Liu L Z, Qu C M, Li J N. 2016. Genome-wide analysis and expression profiling of the SUC and SWEET gene families of sucrose transporters in oilseed rape (Brassica napus L.). Frontiers in Plant Science, 7, 1464.
Julius B T, Leach K A, Tran T M, Mertz R A, Braun D M. 2017. Sugar transporters in plants: New insights and discoveries. Plant and Cell Physiology, 58, 1442–1460.
Keunen E, Peshev D, Vangronsveld J, Van den Ende W, Cuypers A. 2013. Plant sugars are crucial players in the oxidative challenge during abiotic stress: Extending the traditional concept. Plant Cell and Environment, 36, 1242–1255.
Kim D, Landmead B, Salzberg S L. 2015. HISAT: A fast spliced aligner with low memory requirements. Nature Methods, 12, 357–360.
Klemens P A W, Patzke K, Deitmer J, Spinner L, Le Hir R, Bellini C, Bedu M, Chardon F, Krapp A, Neuhaus H E. 2013. Overexpression of the vacuolar sugar carrier AtSWEET16 modifies germination, growth, and stress tolerance in Arabidopsis. Plant Physiology, 163, 1338–1352.
Klemens P A W, Patzke K, Krapp A, Chardon F, Neuhaus H E. 2014. SWEET16 and SWEET17, two novel vacuolar sugar carriers with impact on cellular sugar homeostasis and plant traits. Biochemistry and Cell Biology, 92, 589–589.
Krasensky J, Jonak C. 2012. Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. Journal of Experimental Botany, 63, 1593–1608.
Kryvoruchko I S, Sinharoy S, Torres-Jerez I, Sosso D, Pislariu C I, Guan D, Murray J, Benedito V A, Frommer W B, Udvardi M K. 2016. MtSWEET11, a nodule-specific sucrose transporter of Medicago truncatula. Plant Physiology, 171, 554–565.
Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874.
Lackey J A. 1980. Chromosome numbers in the phaseoleae (Fabaceae:Faboideae) and their relation to taxonomy. American Journal of Botany, 67, 595–602.
Langmead B, Salzberg S L. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods, 9, 357–359.
Leon P, Sheen J. 2003. Sugar and hormone connections. Trends in Plant Science, 8, 110–116.
Li L, Sheen J. 2016. Dynamic and diverse sugar signaling. Current Opinion in Plant Biology, 33, 116–125.
Li P, Zhou H, Shi X, Yu B, Zhou Y, Chen S, Wang Y, Peng Y, Meyer R C, Smeekens S C, Teng S. 2014. The ABI4-induced Arabidopsis ANAC060 transcription factor attenuates ABA signaling and renders seedlings sugar insensitive when present in the nucleus. PLoS Genetics, 10, e1004213.
Lin I W, Sosso D, Chen L Q, Gase K, Kim S G, Kessler D, Klinkenberg P M, Gorder M K, Hou B H, Qu X Q, Carter C J, Baldwin I T, Frommer W B. 2014. Nectar secretion requires sucrose phosphate synthases and the sugar transporter SWEET9. Nature, 508, 546–549.
Liu Q S, Yuan M, Zhou Y, Li X H, Xiao J H, Wang S P. 2011. A paralog of the MtN3/saliva family recessively confers race-specific resistance to Xanthomonas oryzae in rice. Plant Cell and Environment, 34, 1958–1969.
Liu Z L, Adams K L. 2007. Expression partitioning between genes duplicated by polyploidy under abiotic stress and during organ development. Current Biology, 17, 1669–1674.
Liu Z S, Xin M M, Qin J X, Peng H R, Ni Z F, Yao Y Y, Sun Q X. 2015. Temporal transcriptome profiling reveals expression partitioning of homeologous genes contributing to heat and drought acclimation in wheat (Triticum aestivum L.). BMC Plant Biology, 15, 152.
Ljung K, Nemhauser J L, Perata P. 2015. New mechanistic links between sugar and hormone signalling networks. Current Opinion in Plant Biology, 25, 130–137.
Ma Y Y, Zhang Y L, Lu J, Shao H B. 2009. Roles of plant soluble sugars and their responses to plant cold stress. African Journal of Biotechnology, 8, 2004–2010.
Manck-Gotzenberger J, Requena N. 2016. Arbuscular mycorrhiza symbiosis induces a major transcriptional reprogramming of the potato SWEET sugar transporter family. Frontiers in Plant Science, 7, 127.
Matsuoka Y. 2011. Evolution of polyploid Triticum wheats under cultivation: The role of domestication, natural hybridization and allopolyploid speciation in their diversification. Plant and Cell Physiology, 52, 750–764.
Mizuno H, Kasuga S, Kawahigashi H. 2016. The sorghum SWEET gene family: Stem sucrose accumulation as revealed through transcriptome profiling. Biotechnology for Biofuels, 9, 127.
Mizuno H, Kasuga S, Kawahigashi H. 2018. Root lodging is a physical stress that changes gene expression from sucrose accumulation to degradation in sorghum. BMC Plant Biology, 18, 2.
Patil G, Valliyodan B, Deshmukh R, Prince S, Nicander B, Zhao M Z, Sonah H, Song L, Lin L, Chaudhary J, Liu Y, Joshi T, Xu D, Nguyen H T. 2015. Soybean (Glycine max) SWEET gene family: insights through comparative genomics, transcriptome profiling and whole genome re-sequence analysis. BMC Genomics, 16, 520.
Van De Peer Y, Mizrachi E, Marchal K. 2017. The evolutionary significance of polyploidy. Nature Reviews Genetics, 18, 411–424.
Porter K, Worrall W, Gardenhire J, Gilmore E, McDaniel M, Tuleen N. 1987. Registration of ‘TAM 107’ wheat. Crop Science, 27, 818–819.
Ramirez-Gonzalez R H, Borrill P, Lang D, Harrington S A, Brinton J, Venturini L, Davey M, Jacobs J, van Ex F, Pasha A, Khedikar Y, Robinson S J, Cory A T, Florio T, Concia L, Juery C, Schoonbeek H, Steuernagel B, Xiang D, Ridout C J, et?al. 2018. The transcriptional landscape of polyploid wheat. Science, 361, doi: 10.1126/science.aar6089
Robinson M D, McCarthy D J, Smyth G K. 2010. EdgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26, 139–140.
Rolland F, Baena-Gonzalez E, Sheen J. 2006. Sugar sensing and signaling in plants: Conserved and novel mechanisms. Annual Review of Plant Biology, 57, 675–709.
Saitou N, Nei M. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406–425.
Seo P J, Park J M, Kang S K, Kim S G, Park C M. 2011. An Arabidopsis senescence-associated protein SAG29 regulates cell viability under high salinity. Planta, 233, 189–200.
Slama I, Abdelly C, Bouchereau A, Flowers T, Savoure A. 2015. Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Annals of Botany, 115, 433–447.
Sosso D, Luo D P, Li Q B, Sasse J, Yang J L, Gendrot G, Suzuki M, Koch K E, McCarty D R, Chourey P S, Rogowsky P M, Ross-Ibarra J, Yang B, Frommer W B. 2015. Seed filling in domesticated maize and rice depends on SWEET-mediated hexose transport. Nature Genetics, 47, 1489–1493.
Sun S J, Guo S Q, Yang X, Bao Y M, Tang H J, Sun H, Huang J, Zhang H S. 2010. Functional analysis of a novel Cys2/His2-type zinc finger protein involved in salt tolerance in rice. Journal of Experimental Botany, 61, 2807–2818.
Vogel J P, Garvin D F, Mockler T C, Schmutz J, Rokhsar D, Bevan M W, Barry K, Lucas S, Harmon-Smoth M, Lail K, Tice H, Grimwood J, McKenzie N, Huo N, Gu Y Q, Lazo G R, Anderson O D, You F M, Luo M C, Dvorak J, et?al. 2010. Genome sequencing and analysis of the model grass brachypodium distachyon. Nature, 463, 763–768.
Wang Y J, Deng D X, Shi Y T, Miao N, Bian Y L, Yin Z T. 2012. Diversification, phylogeny and evolution of auxin response factor (ARF) family: Insights gained from analyzing maize ARF genes. Molecular Biology Reports, 39, 2401–2415.
Wani S H. 2018. Biochemical, Physiological and Molecular Avenues for Combating Abiotic Stress in Plants. 1st ed. Academic Press, Elsevier Inc.
Xu S M, Liu L X, Woo K C, Wang D L. 2007. Changes in photosynthesis, xanthophyll cycle, and sugar accumulation in two North Australia tropical species differing in leaf angles. Photosynthetica, 45, 348–354.
Yang C W, Zhao L, Zhang H K, Yang Z Z, Wang H, Wen S S, Zhang C Y, Rustgi S, von Wettstein D, Liu B. 2014. Evolution of physiological responses to salt stress in hexaploid wheat. Proceedings of the National Academy of Sciences of the United States of America, 111, 11882–11887.
Yuan M, Zhao J W, Huang R Y, Li X H, Xiao J H, Wang S P. 2014. Rice MtN3/saliva/SWEET gene family: Evolution, expression profiling, and sugar transport. Journal of Integrative Plant Biology, 56, 559–570.
Zhang Y M, Liu Z S, Khan A, Lin Q, Han Y, Mu P, Liu Y G, Zhang H S, Li LY, Meng X H, Ni Z F, Xin M M. 2016. Expression partitioning of homeologs and tandem duplications contribute to salt tolerance in wheat (Triticum aestivum L.). Scientific Reports, 6, 21476.
Zhang Z C, Belcram H, Gornicki P, Charles M, Just J, Huneau C, Magdelenat G, Couloux A, Samain S, Gill B S, Rasmussen J B, Barbe V, Faris J D, Chalhoub B. 2011. Duplication and partitioning in evolution and function of homoeologous Q loci governing domestication characters in polyploid wheat. Proceedings of the National Academy of Sciences of the United States of America, 108, 18737–18742.
 
[1] CHU Jin-peng, GUO Xin-hu, ZHENG Fei-na, ZHANG Xiu, DAI Xing-long, HE Ming-rong. Effect of delayed sowing on grain number, grain weight, and protein concentration of wheat grains at specific positions within spikes[J]. >Journal of Integrative Agriculture, 2023, 22(8): 2359-2369.
[2] FAN Ting-lu, LI Shang-zhong, ZHAO Gang, WANG Shu-ying, ZHANG Jian-jun, WANG Lei, DANG Yi, CHENG Wan-li. Response of dryland crops to climate change and drought-resistant and water-suitable planting technology: A case of spring maize[J]. >Journal of Integrative Agriculture, 2023, 22(7): 2067-2079.
[3] ZHANG Chong, WANG Dan-dan, ZHAO Yong-jian, XIAO Yu-lin, CHEN Huan-xuan, LIU He-pu, FENG Li-yuan, YU Chang-hao, JU Xiao-tang. Significant reduction of ammonia emissions while increasing crop yields using the 4R nutrient stewardship in an intensive cropping system[J]. >Journal of Integrative Agriculture, 2023, 22(6): 1883-1895.
[4] DU Xiang-bei, XI Min, WEI Zhi, CHEN Xiao-fei, WU Wen-ge, KONG Ling-cong. Raised bed planting promotes grain number per spike in wheat grown after rice by improving spike differentiation and enhancing photosynthetic capacity[J]. >Journal of Integrative Agriculture, 2023, 22(6): 1631-1644.
[5] WU Xian-xin, ZANG Chao-qun, ZHANG Ya-zhao, XU Yi-wei, WANG Shu, LI Tian-ya, GAO Li.

Characterization of wheat monogenic lines with known Sr genes and wheat cultivars for resistance to three new races of Puccinia graminis f. sp. tritici in China [J]. >Journal of Integrative Agriculture, 2023, 22(6): 1740-1749.

[6] DONG Xiu-chun, QIAN Tai-feng, CHU Jin-peng, ZHANG Xiu, LIU Yun-jing, DAI Xing-long, HE Ming-rong. Late sowing enhances lodging resistance of wheat plants by improving the biosynthesis and accumulation of lignin and cellulose[J]. >Journal of Integrative Agriculture, 2023, 22(5): 1351-1365.
[7] ZHANG Zhen-zhen, CHENG Shuang, FAN Peng, ZHOU Nian-bing, XING Zhi-peng, HU Ya-jie, XU Fang-fu, GUO Bao-wei, WEI Hai-yan, ZHANG Hong-cheng. Effects of sowing date and ecological points on yield and the temperature and radiation resources of semi-winter wheat[J]. >Journal of Integrative Agriculture, 2023, 22(5): 1366-1380.
[8] LI Jiao-jiao, ZHAO Li, LÜ Bo-ya, FU Yu, ZHANG Shu-fa, LIU Shu-hui, YANG Qun-hui, WU Jun, LI Jia-chuang, CHEN Xin-hong. Development and characterization of a novel common wheat–Mexico Rye T1DL·1RS translocation line with stripe rust and powdery mildew resistance[J]. >Journal of Integrative Agriculture, 2023, 22(5): 1291-1307.
[9] ZHAO Xiao-dong, QIN Xiao-rui, LI Ting-liang, CAO Han-bing, XIE Ying-he. Effects of planting patterns plastic film mulching on soil temperature, moisture, functional bacteria and yield of winter wheat in the Loess Plateau of China[J]. >Journal of Integrative Agriculture, 2023, 22(5): 1560-1573.
[10] JIANG Yun, WANG De-li, HAO Ming, ZHANG Jie, LIU Deng-cai.

Development and characterization of wheat–Aegilops kotschyi 1Uk(1A) substitution line with positive dough quality parameters [J]. >Journal of Integrative Agriculture, 2023, 22(4): 999-1008.

[11] TU Ke-ling, YIN Yu-lin, YANG Li-ming, WANG Jian-hua, SUN Qun. Discrimination of individual seed viability by using the oxygen consumption technique and headspace-gas chromatography-ion mobility spectrometry[J]. >Journal of Integrative Agriculture, 2023, 22(3): 727-737.
[12] Sunusi Amin ABUBAKAR, Abdoul Kader Mounkaila HAMANI, WANG Guang-shuai, LIU Hao, Faisal MEHMOOD, Abubakar Sadiq ABDULLAHI, GAO Yang, DUAN Ai-wang. Growth and nitrogen productivity of drip-irrigated winter wheat under different nitrogen fertigation strategies in the North China Plain[J]. >Journal of Integrative Agriculture, 2023, 22(3): 908-922.
[13] TIAN Jin-yu, LI Shao-ping, CHENG Shuang, LIU Qiu-yuan, ZHOU Lei, TAO Yu, XING Zhi-peng, HU Ya-jie, GUO Bao-wei, WEI Hai-yan, ZHANG Hong-cheng. Increasing the appropriate seedling density for higher yield in dry direct-seeded rice sown by a multifunctional seeder after wheat-straw return[J]. >Journal of Integrative Agriculture, 2023, 22(2): 400-416.
[14] HU Wen-jing, FU Lu-ping, GAO De-rong, LI Dong-sheng, LIAO Sen, LU Cheng-bin. Marker-assisted selection to pyramid Fusarium head blight resistance loci Fhb1 and Fhb2 in a high-quality soft wheat cultivar Yangmai 15[J]. >Journal of Integrative Agriculture, 2023, 22(2): 360-370.
[15] Zaid CHACHAR, Siffat Ullah KHAN, ZHANG Xue-huan, LENG Peng-fei, ZONG Na, ZHAO Jun. Characterization of transgenic wheat lines expressing maize ABP7 involved in kernel development[J]. >Journal of Integrative Agriculture, 2023, 22(2): 389-399.
No Suggested Reading articles found!