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Journal of Integrative Agriculture  2023, Vol. 22 Issue (6): 1720-1739    DOI: 10.1016/j.jia.2023.04.031
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Molecular characterization of the SAUR gene family in sweet cherry and functional analysis of PavSAUR55 in the process of abscission
HOU Qian-dong1*, HONG Yi1*, WEN Zhuang1, SHANG Chun-qiong2, LI Zheng-chun2, CAI Xiao-wei1, QIAO Guang1, WEN Xiao-peng1#

1 Key Laboratory of Plant Resource Conservation and Germplasm Innovation in Mountainous Region (Ministry of Education), College of Life Sciences/Institute of Agro-bioengineering, Guizhou University, Guiyang 550025, P.R.China

2 College of Forestry/Institute for Forest Resources & Environment of Guizhou, Guizhou University, Guiyang 550025, P.R.China

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摘要  

小生长素上调RNASAUR)是一个广泛分布于陆地植物中较大的一个基因家族。本研究对甜樱桃中的SAUR家族进行了综合分析,并利用遗传转化的方法鉴定了PavSAUR55的潜在生物学功能。甜樱桃基因组编码86SAUR成员,其中大多数是无内含子的。进化上这些基因被分为七个亚类。基因复制事件表明甜樱桃基因组中发生了片段重复和串联重复事件。大多数成员在进化过程中主要经历纯化选择压力。在果实发育过程中,PavSAUR16/45/56/63的表达水平上调,PavSAUR12/61的表达水平下调。由于PavSAUR13/16/55/61在小果脱落过程中的显著差异表达,它们可能是参与调节甜樱桃生理性果实脱落的候选基因。PavSAUR55在拟南芥中的过表达产生了更早的生殖生长、根系伸长和延迟的花瓣脱落。此外,该基因并不会导致种子发芽时间的改变,并且能够在ABA处理下增加侧根的数量。这些结果表明,甜樱桃SAURs在小果脱落过程中起着重要的作用,并将有助于未来深入了解该果树中可能发生的严重小果脱落的机制奠定基础。



Abstract  

Small auxin up RNA (SAUR) is a large gene family that is widely distributed among land plants.  In this study, a comprehensive analysis of the SAUR family was performed in sweet cherry, and the potential biological functions of PavSAUR55 were identified using the method of genetic transformation.  The sweet cherry genome encodes 86 SAUR members, the majority of which are intron-less.  These genes appear to be divided into seven subfamilies through evolution.  Gene duplication events indicate that fragment duplication and tandem duplication events occurred in the sweet cherry.  Most of the members mainly underwent purification selection pressure during evolution.  During fruit development, the expression levels of PavSAUR16/45/56/63 were up-regulated, and conversely, those of PavSAUR12/61 were down-regulated.  Due to the significantly differential expressions of PavSAUR13/16/55/61 during the fruitlet abscission process, they might be the candidate genes involved in the regulation of physiological fruit abscission in sweet cherry.  Overexpression of PavSAUR55 in Arabidopsis produced earlier reproductive growth, root elongation, and delayed petal abscission.  In addition, this gene did not cause any change in the germination time of seeds and was able to increase the number of lateral roots under abscisic acid (ABA) treatment.  The identified SAURs of sweet cherry play a crucial role in fruitlet abscission and will facilitate future insights into the mechanism underlying the heavy fruitlet abscission that can occur in this fruit crop.

Keywords:  sweet cherry        small auxin up RNA        gene family        expression profile        fruitlet abscission  
Received: 16 September 2022   Online: 28 April 2023   Accepted: 24 March 2023
Fund: This project was supported by grants from the National Natural Science Foundation of China (32272649) and the Core Program of Guizhou Education Department, China (KY 2021-038).
About author:  HOU Qian-dong, E-mail: qiandhou@163.com; HONG Yi, E-mail: hongyi715@163.com; #Correspondence WEN Xiao-peng, E-mail: xpwensc@hotmail.com *These authors contributed equally to this work.

Cite this article: 

HOU Qian-dong, HONG Yi, WEN Zhuang, SHANG Chun-qiong, LI Zheng-chun, CAI Xiao-wei, QIAO Guang, WEN Xiao-peng. 2023. Molecular characterization of the SAUR gene family in sweet cherry and functional analysis of PavSAUR55 in the process of abscission. Journal of Integrative Agriculture, 22(6): 1720-1739.

Baez R R, Nemhauser J L. 2021. Expansion and innovation in auxin signaling: Where do we grow from here? Development148, dev187120.

Bailey T L, Boden M, Buske F A, Frith M, Grant C E, Clementi L, Ren J, Li W W, Noble W S. 2009. MEME Suite: Tools for motif discovery and searching. Nucleic Acids Research37, 1–7.

Bing L, Rojas P, Perez J, Villar L, Lienqueo I, Correa F, Sagredo B, Masciarelli O, Luna V. 2020. Comparative transcriptomic analysis reveals novel roles of transcription factors and hormones during the flowering induction and floral bud differentiation in sweet cherry trees. PLoS ONE15, 1–28.

Chen C, Chen H, Zhang Y, Thomas H R, Frank M H, He Y, Xia R. 2020. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Molecular Plant13, 1194–1202.

Chen Y, Hao X, Cao J. 2014. Small auxin upregulated RNA (SAUR) gene family in maize: Identification, evolution, and its phylogenetic comparison with Arabidopsis, rice, and sorghum. Journal of Integrative Plant Biology56, 133–150.

Cheng S, Xian W, Fu Y, Marin B, Keller J, Wu T, Sun W, Li X, Xu Y, Zhang Y, Wittek S, Reder T, Günther G, Gontcharov A, Wang S, Li L, Liu X, Wang J, Yang H, Xu X, et al. 2019. Genomes of subaerial zygnematophyceae provide insights into land plant evolution. Cell179, 1057–1067.

Dong J, Sun N, Yang J, Deng Z, Lan J, Qin G, He H, Deng X W, Irish V F, Chen H, Wei N. 2019. The transcription factors TCP4 and PIF3 antagonistically regulate organ-specific light induction of SAUR genes to modulate cotyledon opening during de-etiolation in Arabidopsis. Plant Cell31, 1155–1170.

Flores-Sandoval E, Eklund D M, Bowman J L. 2015. A simple auxin transcriptional response system regulates multiple morphogenetic processes in the liverwort Marchantia polymorphaPLoS Genetics11, 1–26.

Gastaldi V, Lucero L E, Ferrero L V, Ariel F D, Gonzalez D H. 2020. Class-I TCP transcription factors activate the SAUR63 gene subfamily in gibberellin-dependent stamen filament elongation. Plant Physiology182, 2096–2110.

Guo K B, Qiao G, Qiu Z L, Wen Z, Yang H, Wen X P. 2020. The fruit dropping characters of sweet cherry and its interior causes in insufficient chilling zone. Russian Journal of Plant Physiology67, 94–102.

Hu W, Yan H, Luo S, Pan F, Wang Y, Xiang Y. 2018. Genome-wide analysis of poplar SAUR gene family and expression profiles under cold, polyethylene glycol and indole-3-acetic acid treatments. Plant Physiology and Biochemistry128, 50–65.

Huang X, Bao Y, Wang B, Liu L J, Chen J, Dai L J, Baloch S U, Peng D X. 2016. Identification of small auxin-up RNA (SAUR) genes in Urticales plants: Mulberry (Morus notabilis), hemp (Cannabis sativa) and ramie (Boehmeria nivea). Journal of Genetics95, 119–129.

Jain M, Tyagi A K, Khurana J P. 2006. Genome-wide analysis, evolutionary expansion, and expression of early auxin-responsive SAUR gene family in rice (Oryza sativa). Genomics88, 360–371.

Jin X, Zimmermann J, Polle A, Fischer U. 2015. Auxin is a long-range signal that acts independently of ethylene signaling on leaf abscission in PopulusFrontiers in Plant Science6, 1–10.

Kato H, Nishihama R, Weijers D, Kohchi T. 2018. Evolution of nuclear auxin signaling: Lessons from genetic studies with basal land plants. Journal of Experimental Botany69, 291–301.

Koch M A, Haubold B, Mitchell-Olds T. 2000. Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in ArabidopsisArabis, and related genera (Brassicaceae). Molecular Biology and Evolution17, 1483–1498.

Kuang J F, Wu J Y, Zhong H Y, Li C Q, Chen J Y, Lu W J, Li J G. 2012. Carbohydrate stress affecting fruitlet abscission and expression of genes related to auxin signal transduction pathway in litchi. International Journal of Molecular Sciences13, 16084–16103.

Landis J B, Soltis D E, Li Z, Marx H E, Barker M S, Tank D C, Soltis P S. 2018. Impact of whole-genome duplication events on diversification rates in angiosperms. American Journal of Botany105, 348–363.

Lau S, Shao N, Bock R, Jürgens G, De Smet I. 2009. Auxin signaling in algal lineages, fact or myth? Trends in Plant Science14, 182–188.

Lespinet O, Wolf Y I, Koonin E V, Aravind L. 2002. The role of lineage-specific gene family expansion in the evolution of eukaryotes. Genome Research12, 1048–1059.

Li X, Liu G, Geng Y, Wu M, Pei W, Zhai H, Zang X, Li X, Zhang J, Yu S, Yu J. 2017. A genome-wide analysis of the small auxin-up RNA (SAUR) gene family in cotton. BMC Genomics18, 1–22.

Li Y, Liu Z B, Shi X, Hagen G, Guilfoyle T J. 1994. An auxin-inducible element in soybean SAUR promoters. Plant Physiology106, 37–43.

Li Z G, Chen H W, Li Q T, Tao J J, Bian X H, Ma B, Zhang W K, Chen S Y, Zhang J S. 2015. Three SAUR proteins SAUR76, SAUR77 and SAUR78 promote plant growth in ArabidopsisScientific Reports5, 1–19.

Liu J, Shi M, Wang J, Zhang B, Li Y, Wang J, El-Sappah A H, Liang Y. 2020. Comparative transcriptomic analysis of the development of sepal morphology in tomato (Solanum lycopersicum L.). International Journal of Molecular Sciences21, 1–23.

Luo J, Zhou J J, Zhang J Z. 2018. Aux/IAA gene family in plants: Molecular structure, regulation, and function. International Journal of Molecular Sciences19, 1–17.

Ma C, Jiang C Z, Gao J. 2021. Regulatory mechanisms underlying activation of organ abscission. Annual Plant Reviews Online4, 27–56.

Mastrangelo A M, Marone D, Laidò G, De Leonardis A M, De Vita P. 2012. Alternative splicing: Enhancing ability to cope with stress via transcriptome plasticity. Plant Science185–186, 40–49.

van Mourik H, van Dijk A D J, Stortenbeker N, Angenent G C, Bemer M. 2017. Divergent regulation of Arabidopsis SAUR genes, A focus on the SAUR10-clade. BMC Plant Biology17, 1–14.

Mutte S K, Kato H, Rothfels C, Melkonian M, Wong G K S, Weijers D. 2018. Origin and evolution of the nuclear auxin response system. Elife7, e33399.

Paponov I A, Paponov M, Teale W, Menges M, Chakrabortee S, Murray J A H, Palme K. 2008. Comprehensive transcriptome analysis of auxin responses in ArabidopsisMolecular Plant1, 321–337.

Patharkar O R, Walker J C. 2018. Advances in abscission signaling. Journal of Experimental Botany69, 733–740.

Qiu Z, Wen Z, Hou Q, Qiao G, Yang K, Hong Y, Wen X. 2021. Cross-talk between transcriptome, phytohormone and HD-ZIP gene family analysis illuminates the molecular mechanism underlying fruitlet abscission in sweet cherry (Prunus avium L.). BMC Plant Biolology21, 1–18.

Rayle D L, Cleland R E. 1980. Auxin-induced growth of soybean. Plant Physiology66, 433–437.

Ren H, Gray W M. 2015. SAUR proteins as effectors of hormonal and environmental signals in plant growth. Molecular Plant8, 1153–1164.

Ren H, Park M Y, Spartz A K, Wong J H, Gray W M. 2018. A subset of plasma membrane-localized PP2C.D phosphatases negatively regulate SAUR-mediated cell expansion in Arabidopsis. PLoS Genetics14, 1–27.

Rensing S A, Lang D, Zimmer A D, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud P F, Lindquist E A, Kamisugi Y, Tanahashi T, Sakakibara K, Fujita T, Oishi K, Shin I T, Kuroki Y, Toyoda A, Suzuki Y, Hashimoto S I, Yamaguchi K, et al. 2008. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science319, 64–69.

Roberts J A, Elliott K A, Gonzalez-Carranza Z H. 2002. Abscission, dehiscence, and other cell separation processes. Annual Review of Plant Biology53, 131–158.

Rogozin I B, Sverdlov A V, Babenko V N, Koonin E V. 2005. Analysis of evolution of exon–intron structure of eukaryotic genes. Briefings in Bioinformatics6, 118–134.

Rose A B, Carter A, Korf I, Kojima N. 2016. Intron sequences that stimulate gene expression in ArabidopsisPlant Molecular Biology, 92, 337–346.

Roy S W, Gilbert W. 2006. The evolution of spliceosomal introns: patterns, puzzles and progress. Nature Reviews Genetics7, 211–221.

Schmittgen T D, Livak K J. 2008. Analyzing real-time PCR data by the comparative CT method. Nature Protocols3, 1101–1108.

Shin J H, Mila I, Liu M, Rodrigues M A, Vernoux T, Pirrello J, Bouzayen M. 2019. The RIN-regulated Small Auxin-Up RNA SAUR69 is involved in the unripe-to-ripe phase transition of tomato fruit via enhancement of the sensitivity to ethylene. New Phytologist222, 820–836.

Shirasawa K, Isuzugawa K, Ikenaga M, Saito Y, Yamamoto T, Hirakawa H, Isobe S. 2017. The genome sequence of sweet cherry (Prunus avium) for use in genomics-assisted breeding. DNA Research24, 499–508.

Soltis P S, Soltis D E. 2016. Ancient WGD events as drivers of key innovations in angiosperms. Current Opinion in Plant Biology30, 159–165.

Spartz A K, Lee S H, Wenger J P, Gonzalez N, Itoh H, Inzé D, Peer W A, Murphy A S, Overvoorde P J, Gray W M. 2012. The SAUR19 subfamily of SMALL AUXIN UP RNA genes promote cell expansion. Plant Journal70, 978–990.

Spartz A K, Ren H, Park M Y, Grandt K N, Lee S H, Murphy A S, Sussman M R, Overvoorde P J, Gray W M. 2014. SAUR inhibition of PP2C-D phosphatases activates plasma membrane H+-ATPases to promote cell expansion in ArabidopsisPlant Cell26, 2129–2142.

Stortenbeker N, Bemer M. 2019. The SAUR gene family, The plant’s toolbox for adaptation of growth and development. Journal of Experimental Botany70, 17–27.

Tranbarger T J, Tadeo F R. 2020. Diversity and functional dynamics of fleshy fruit abscission zones. Annual Plant Reviews Online3, 151–214.

Wang J, Liu W, Zhu D, Hong P, Zhang S, Xiao S, Tan Y, Chen X, Xu L, Zong X, Zhang L, Wei H, Yuan X, Liu Q. 2020. Chromosome-scale genome assembly of sweet cherry (Prunus avium L.) cv. Tieton obtained using long-read and Hi-C sequencing. Horticulture Research7, 122.

Wang P, Lu S, Xie M, Wu M, Ding S, Khaliq A, Ma Z, Mao J, Chen B, 2020. Identification and expression analysis of the small auxin-up RNA (SAUR) gene family in apple by inducing of auxin. Gene750, 144725.

Wang S, Li L, Li H, Sahu S K, Wang H, Xu Y, Xian W, Song B, Liang H, Cheng S, Chang Y, Song Y, Çebi Z, Wittek S, Reder T, Peterson M, Yang H, Wang J, Melkonian B, Van de Peer Y, et al. 2020. Genomes of early-diverging streptophyte algae shed light on plant terrestrialization. Nature Plants6, 95–106.

Wang X, Yu R, Wang J, Lin Z, Han X, Deng Z, Fan L, He H, Deng X W, Chen H. 2020. The asymmetric expression of SAUR genes mediated by ARF7/19 promotes the gravitropism and phototropism of plant hypocotyls. Cell Reports31, 107529.

Wang Y, Tang H, Debarry J D, Tan X, Li J, Wang X, Lee T H, Jin H, Marler B, Guo H, Kissinger J C, Paterson A H. 2012. MCScanX, A toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Research40, 1–14.

Wei H, Chen X, Zong X, Shu H, Gao D, Liu Q. 2015. Comparative transcriptome analysis of genes involved in anthocyanin biosynthesis in the red and yellow fruits of sweet cherry (Prunus avium L.). PLoS ONE10, 1–20.

Wong J H, Klejchová M, Snipes A, Nagpal P, Bak G, Wang B, Dunlap S, Park Y, Kunkel N, Trinidad B, Reed W, Blatt R, Gray W M. 2021. SAUR proteins and PP2C.D phosphatases regulate H+-ATPases and K+ channels to control stomatal movements. Plant Physiology185, 256–273.

Wong J H, Spartz A K, Park M Y, Du M, Gray W M. 2019. Mutation of a conserved motif of PP2C.D phosphatases confers SAUR immunity and constitutive activity. Plant Physiology181, 353–366.

Xie R, Dong C, Ma Y, Deng L, He S, Yi S, Lv Q, Zheng Y. 2015. Comprehensive analysis of SAUR gene family in citrus and its transcriptional correlation with fruitlet drop from abscission zone A. Functional & Integrative Genomics15, 729–740.

Yang S, Zhang X, Yue J X, Tian D, Chen J Q. 2008. Recent duplications dominate NBS-encoding gene expansion in two woody species. Molecular Genetics and Genomics280, 187–198.

Zhang H, Yu Z, Yao X, Chen J, Chen X, Zhou H, Lou Y, Ming F, Jin Y. 2021. Genome-wide identification and characterization of small auxin-up RNA (SAUR) gene family in plants: Evolution and expression profiles during normal growth and stress response. BMC Plant Biology21, 1–14.

Zhang N, Huang X, Bao Y, Wang B, Zeng H, Cheng W, Tang M, Li Y, Ren J, Sun Y. 2017. Genome-wide identification of SAUR genes in watermelon (Citrullus lanatus). Physiology and Molecular Biology of Plants23, 619–628.

Zhao Y. 2018. Essential roles of local auxin biosynthesis in plant development and in adaptation to environmental changes. Annual Review of Plant Biology69, 417–435.

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