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Journal of Integrative Agriculture  2025, Vol. 24 Issue (2): 564-574    DOI: 10.1016/j.jia.2024.07.014
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Functional analysis of tomato MAP65 gene family, highlighting SlMAP65-1’s role in fruit morphogenesis

Peiyu Zhang1, Guoning Zhu1, Chunjiao Zhang2#, Hongliang Zhu1#

1 College of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100083, China

2 Supervision, Inspection & Testing Center of Agricultural Products Quality, Ministry of Agriculture and Rural Affairs, Beijing 100083, China

 Highlights 
Nine SlMAP65 family genes were identified in the tomato genome.
SlMAP65-1 is involved in fruit morphogenesis at the early fruit development stage.

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摘要  

植物的生长发育过程伴随着微管的动态变化,而微管阵列的重排受多种微管结合蛋白(microtubule-associated proteins , MAPs)的调控。植物中的MAP65蛋白在一些物种中已经得到了详尽的表征,但有关番茄(Solanum lycopersicum)中 MAP65 家族成员的信息还很有限。本研究在番茄基因组中鉴定到 9 个 SlMAP65 基因家族成员。对 SlMAP65 家族成员的理化性质、亲缘关系、保守基序、结构域、基因结构和顺式调控元件等进行了系统分析。然后利用 CRISPR/Cas9 技术在番茄中敲除了相对表达量最高的成员SlMAP65-1。结果表明,slmap65-1突变体果实果形指数显著增加,SlMAP65-1在果实发育早期参与了果实的形态发生。这些结果为番茄果实形态建成相关研究领域以及未来SlMAP65家族成员的功能研究提供了新信息。



Abstract  
The plant growth process is accompanied by dynamic changes in the microtubules, and the rearrangement of microtubules is regulated by diverse microtubule-associated proteins (MAPs).  Plant MAP65s have been exhaustively characterized in some species, but the information about MAP65 family members in tomato (Solanum lycopersicum) is limited.  In this study, nine SlMAP65 family genes were identified in the tomato genome.  Then a systematic analysis that considered the physio-chemical properties, evolution, conserved motifs, domains, gene structure, and cis-regulatory elements of SlMAP65 family members was conducted.  The family member SlMAP65-1, which had the highest expression, was knocked out by CRISPR/Cas9.  The tomato fruit of slmap65-1 loss of function lines showed an elongated morphology, and the data indicated that SlMAP65-1 is involved in fruit morphogenesis at the early fruit development stage.  These results provide new insights for fruit morphogenesis-related research and future functional studies of the SlMAP65 family members in tomato.


Keywords:  tomato       MAP65 family        fruit shape        microtubule organization  
Received: 18 September 2024   Accepted: 02 April 2024
Fund: 
This work was supported by the National Natural Sciences Foundation of China (32302623 and 32172639).
About author:  Peiyu Zhang, E-mail: zhangpy979@163.com; #Correspondence Chunjiao Zhang, E-mail: cc15809181@163.com; Hongliang Zhu, E-mail: hlzhu@cau.edu.cn

Cite this article: 

Peiyu Zhang, Guoning Zhu, Chunjiao Zhang, Hongliang Zhu. 2025. Functional analysis of tomato MAP65 gene family, highlighting SlMAP65-1’s role in fruit morphogenesis. Journal of Integrative Agriculture, 24(2): 564-574.

Bailey T L, Johnson J, Grant C E, Noble W S. 2015. The MEME suite. Nucleic Acids Research43, W39–W49.

Bao Z R, Guo Y, Deng Y L, Zang J Z, Zhang J H, Deng Y T, Ouyang B, Qu X L, Bürstenbinder K, Wang P W. 2023. Microtubule-associated protein SlMAP70 interacts with IQ67-domain protein SlIQD21a to regulate fruit shape in tomato. Plant Cell35, koad231.

Bodakuntla S, Jijumon A S, Villablanca C, Gonzalez-Billault C, Janke C. 2019. Microtubule-associated proteins: Structuring the cytoskeleton. Trends in Cell Biology29, 804–819.

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

Chen Y, Liu X Y, Zhang W J, Li J, Liu H F, Yang L, Lei P, Zhang H C, Yu F. 2022. MOR1/MAP215 acts synergistically with katanin to control cell division and anisotropic cell elongation in Arabidopsis. Plant Cell34, 3006–3027.

Cong B, Barrero L S, Tanksley S D. 2008. Regulatory change in YABBY-like transcription factor led to evolution of extreme fruit size during tomato domestication. Nature Genetics40, 800–804.

Deng J, Wang X F, Liu Z Q, Mao T L. 2021. The microtubule-associated protein WDL4 modulates auxin distribution to promote apical hook opening in Arabidopsis. Plant Cell33, 1927–1944.

Gardiner J. 2013. The evolution and diversification of plant microtubule-associated proteins. Plant Journal75, 219–229.

Glotzer M, Murray A W, Kirschner M W. 1991. Cyclin is degraded by the ubiquitin pathway. Nature349, 132–138.

Guo L B, Ho C M K, Kong Z S, Lee Y R J, Qian Q, Liu B. 2009. Evaluating the microtubule cytoskeleton and its interacting proteins in monocots by mining the rice genome. Annals of Botany103, 387–402.

Hamada T. 2014. Microtubule organization and microtubule-associated proteins in plant cells. International Review of Cell and Molecular Biology312, 1–52.

Hsiao A S, Huang J Y. 2023. Microtubule regulation in plants: From morphological development to stress adaptation. Biomolecules13, 627.

Hussey P J, Hawkins T J, Igarashi H, Kaloriti D, Smertenko A. 2002. The plant cytoskeleton: Recent advances in the study of the plant microtubule-associated proteins MAP-65, MAP-190 and the Xenopus MAP215-like protein, MOR1. Plant Molecular Biology50, 915–924.

Jiang C J, Sonobe S. 1993. Identification and preliminary characterization of a 65-Kda higher-plant microtubule-associated protein. Journal of Cell Science105, 891–901.

Koga H, Kojima M, Takebayashi Y, Sakakibara H, Tsukaya H. 2021. Identification of the unique molecular framework of heterophylly in the amphibious plant Callitriche palustris L. Plant Cell33, 3272–3292.

Krtková J, Benáková M, Schwarzerová K. 2016. Multifunctional microtubule-associated proteins in plants. Frontiers in Plant Science7, 474.

Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution35, 1547–1549.

Li H, Sun B J, Sasabe M, Deng X G, Machida Y, Lin H H, Lee Y R J, Liu B. 2017. Arabidopsis MAP65-4 plays a role in phragmoplast microtubule organization and marks the cortical cell division site. New Phytologist215, 187–201.

Li H, Zeng X, Liu Z Q, Meng Q T, Yuan M, Mao T L. 2009. Arabidopsis microtubule-associated protein AtMAP65-2 acts as a microtubule stabilizer. Plant Molecular Biology69, 313–324.

Li N, He Q, Wang J, Wang B K, Zhao J T, Huang S Y, Yang T, Tang Y P, Yang S B, Aisimutuola P, Xu R Q, Hu J H, Jia C P, Ma K, Li Z Q, Jiang F L, Gao J, Lan H Y, Zhou Y F, Zhang X Y, et al. 2023. Super-pangenome analyses highlight genomic diversity and structural variation across wild and cultivated tomato species. Nature Genetics55, 852–860.

Li R, Li R, Li X D, Fu D Q, Zhu B Z, Tian H Q, Luo Y B, Zhu H L. 2018. Multiplexed CRISPR/Cas9-mediated metabolic engineering of gamma-aminobutyric acid levels in Solanum lycopersicumPlant Biotechnology Journal16, 415–427.

Liu J P, Van Eck J, Cong B, Tanksley S D. 2002. A new class of regulatory genes underlying the cause of pear-shaped tomato fruit. Proceedings of the National Academy of Sciences of the United States of America99, 13302–13306.

Livanos P, Muller S. 2019. Division plane establishment and cytokinesis. Annual Review of Plant Biology70, 239–267.

Lloyd C, Chan J. 2004. Microtubules and the shape of plants to come. Nature Reviews Molecular Cell Biology5, 13–22.

Lucas J R, Courtney S, Hassfurder M, Dhingra S, Bryant A, Shaw S L. 2011. Microtubule-associated proteins MAP65-1 and MAP65-2 positively regulate axial cell growth in etiolated Arabidopsis hypocotyls. Plant Cell23, 1889–1903.

Marchler-Bauer A, Bryant S H. 2004. CD-Search: Protein domain annotations on the fly. Nucleic Acids Research32, W327–W331.

Martin C, Bhatt K, Baumann K. 2001. Shaping in plant cells. Current Opinion in Plant Biology4, 540–549.

Mills A M, Morris V H, Rasmussen C G. 2022. The localization of PHRAGMOPLAST ORIENTING KINESIN1 at the division site depends on the microtubule-binding proteins TANGLED1 and AUXIN-INDUCED IN ROOT CULTURES9 in Arabidopsis. The Plant Cell34, 4583–4599.

Monforte A J, Diaz A, Cano-Delgado A, van der Knaap E. 2014. The genetic basis of fruit morphology in horticultural crops: Lessons from tomato and melon. Journal of Experimental Botany65, 4625–4637.

Muller S, Smertenko A, Wagner V, Heinrich M, Hussey P J, Hauser M T. 2004. The plant microtubule-associated protein AtMAP65-3/PLE is essential for cytokinetic phragmoplast function. Current Biology14, 412–417.

Munos S, Ranc N, Botton E, Berard A, Rolland S, Duffe P, Carretero Y, Le Paslier M C, Delalande C, Bouzayen M, Brunel D, Causse M. 2011. Increase in tomato locule number is controlled by two single-nucleotide polymorphisms located near WUSCHELPlant Physiology156, 2244–2254.

Nakamura M, Ehrhardt D W, Hashimoto T. 2010. Microtubule and katanin-dependent dynamics of microtubule nucleation complexes in the acentrosomal Arabidopsis cortical array. Nature Cell Biology12, U1064–U1070.

Paradez A, Wright A, Ehrhardt D W. 2006. Microtubule cortical array organization and plant cell morphogenesis. Current Opinion in Plant Biology9, 571–578.

Peaucelle A, Wightman R, Hofte H. 2015. The control of growth symmetry breaking in the Arabidopsis hypocotyl. Current Biology25, 1746–1752.

Quentin M, Baures I, Hoefle C, Caillaud M C, Allasia V, Panabieres F, Abad P, Huckelhoven R, Keller H, Favery B. 2016. The Arabidopsis microtubule-associated protein MAP65-3 supports infection by filamentous biotrophic pathogens by down-regulating salicylic acid-dependent defenses. Journal of Experimental Botany67, 1731–1743.

Rasmussen C G, Wright A J, Muller S. 2013. The role of the cytoskeleton and associated proteins in determination of the plant cell division plane. Plant Journal75, 258–269.

Rodriguez G R, Munos S, Anderson C, Sim S C, Michel A, Causse M, Gardener B B M, Francis D, van der Knaap E. 2011. Distribution of SUNOVATELC, and FAS in the tomato germplasm and the relationship to fruit shape diversity. Plant Physiology156, 275–285.

Sato S, Tabata S, Hirakawa H, Asamizu E, Shirasawa K, Isobe S, Kaneko T, Nakamura Y, Shibata D, Aoki K, Egholm M, Knight J, Bogden R, Li C B, Shuang Y, Xu X, Pan S K, Cheng S F, Liu X, Ren Y Y, et al. 2012. The tomato genome sequence provides insights into fleshy fruit evolution. Nature485, 635–641.

Smertenko A P, Kaloriti D, Chang H Y, Fiserova J, Opatrny Z, Hussey P J. 2008. The C-terminal variable region specifies the dynamic properties of Arabidopsis microtubule-associated protein MAP65 isotypes. Plant Cell20, 3346–3358.

Xiao H, Jiang N, Schaffner E, Stockinger E J, van der Knaap E. 2008. A retrotransposon-mediated gene duplication underlies morphological variation of tomato fruit. Science319, 1527–1530.

Zang J Z, Klemm S, Pain C, Duckney P, Bao Z R, Stamm G, Kriechbaumer V, Burstenbinder K, Hussey P J, Wang P W. 2021. A novel plant actin-microtubule bridging complex regulates cytoskeletal and ER structure at ER-PM contact sites. Current Biology31, 1251–1260.e4.

Zhao F, Du F, Oliveri H, Zhou L W, Ali O, Chen W Q, Feng S L, Wang Q Q, Lu S Q, Long M, Schneider R, Sampathkumar A, Godin C, Traas J, Jiao Y L. 2020. Microtubule-mediated wall anisotropy contributes to leaf blade flattening. Current Biology30, 3972–3985.e6.

Zhu Y, Liu W J, Sheng Y, Zhang J, Chiu T Y, Yan J W, Jiang M Y, Tan M P, Zhang A. 2015. ABA affects brassinosteroid-induced antioxidant defense via ZmMAP65-1a in maize plants. Plant and Cell Physiology56, 1442–1455.

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