Organelle Ca
Ca2+/CAM1-SELTP interaction
Gossypium hirsutum L.
amyloplast-plasmodesmata organelle
intracellular activation and intercellular transformation
plant regeneration
somatic cell totipotency
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
19 Mar 2024
19 Mar 2024
Historique:
received:
13
01
2024
accepted:
20
02
2024
medline:
19
3
2024
pubmed:
19
3
2024
entrez:
19
3
2024
Statut:
aheadofprint
Résumé
Somatic cell totipotency in plant regeneration represents the forefront of the compelling scientific puzzles and one of the most challenging problems in biology. How somatic embryogenic competence is achieved in regeneration remains elusive. Here, we discover uncharacterized organelle-based embryogenic differentiation processes of intracellular acquisition and intercellular transformation, and demonstrate the underlying regulatory system of somatic embryogenesis-associated lipid transfer protein (SELTP) and its interactor calmodulin1 (CAM1) in cotton as the pioneer crop for biotechnology application. The synergistic CAM1 and SELTP exhibit consistent dynamical amyloplast-plasmodesmata (PD) localization patterns but show opposite functional effects. CAM1 inhibits the effect of SELTP to regulate embryogenic differentiation for plant regeneration. It is noteworthy that callus grafting assay reflects intercellular trafficking of CAM1 through PD for embryogenic transformation. This work originally provides insight into the mechanisms responsible for embryogenic competence acquisition and transformation mediated by the Ca
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Modern Agro-industry Technology Research System of Shandong Province
ID : SDAIT-03-02
Organisme : Shandong Province Excellent Youth Fund
ID : ZR2023YQ022
Organisme : National Natural Science Foundation of China
ID : 32372142
Organisme : National Natural Science Foundation of China
ID : 32001589
Organisme : Young Elite Scientists Sponsorship Program by CAST
ID : 2022QNRC001
Informations de copyright
© 2024 The Authors. New Phytologist © 2024 New Phytologist Foundation.
Références
Anil VS, Rao KS. 2000. Calcium-mediated signaling during sandalwood somatic embryogenesis. Role for exogenous calcium as second messenger. Plant Physiology 123: 1301-1312.
Burch-Smith TM, Stonebloom S, Xu M, Zambryski PC. 2011. Plasmodesmata during development: re-examination of the importance of primary, secondary, and branched plasmodesmata structure versus function. Protoplasma 248: 61-74.
Bustillo-Avendaño E, Ibáñez S, Sanz O, Sousa Barros JA, Gude I, Perianez-Rodriguez J, Micol JL, Del Pozo JC, Moreno-Risueno MA, Pérez-Pérez JM. 2018. Regulation of hormonal control, cell reprogramming, and patterning during de novo root organogenesis. Plant Physiology 176: 1709-1727.
Calabuig-Serna A, Mir R, Arjona P, Seguí-Simarro JM. 2023. Calcium dynamics and modulation in carrot somatic embryogenesis. Frontiers in Plant Science 14: 1150198.
Condic ML. 2014. Totipotency: what it is and what it is not. Stem Cells and Development 23: 796-812.
Da Silva FCV, do Nascimento VV, Machado OLT, Pereira LDS, Gomes VM, de Oliveira Carvalho A. 2018. Insight into the α-amylase inhibitory activity of plant lipid transfer proteins. Journal of Chemical Information and Modeling 58: 2294-2304.
Deng J, Sun W, Zhang B, Sun S, Xia L, Miao Y, He L, Lindsey K, Yang X, Zhang X. 2022. GhTCE1-GhTCEE1 dimers regulate transcriptional reprogramming during wound-induced callus formation in cotton. Plant Cell 34: 4554-4568.
Denninger P, Bleckmann A, Lausser A, Vogler F, Ott T, Ehrhardt DW, Frommer WB, Sprunck S, Dresselhaus T, Grossmann G. 2014. Male-female communication triggers calcium signatures during fertilization in Arabidopsis. Nature Communications 5: 4645.
Diz MS, Carvalho AO, Ribeiro SF, Da Cunha M, Beltramini L, Rodrigues R, Nascimento VV, Machado OL, Gomes VM. 2011. Characterisation, immunolocalisation and antifungal activity of a lipid transfer protein from chili pepper (Capsicum annuum) seeds with novel α-amylase inhibitory properties. Physiologia Plantarum 142: 233-246.
Earley KW, Haag JR, Pontes O, Opper K, Juehne T, Song K, Pikaard CS. 2006. Gateway-compatible vectors for plant functional genomics and proteomics. The Plant Journal 45: 616-629.
Fehér A. 2019. Callus, dedifferentiation, totipotency, somatic embryogenesis: what these terms mean in the era of molecular plant biology? Frontiers in Plant Science 10: 536.
Feng MQ, Jiang N, Wang PB, Liu Y, Xia QM, Jia HH, Shi QF, Long JM, Xiao GA, Yin ZP et al. 2023. miR171-targeted SCARECROW-LIKE genes CsSCL2 and CsSCL3 regulate somatic embryogenesis in citrus. Plant Physiology 192: 2838-2854.
Feng Q, Xiao L, He Y, Liu M, Wang J, Tian S, Zhang X, Yuan L. 2021. Highly efficient, genotype-independent transformation and gene editing in watermelon (Citrullus lanatus) using a chimeric ClGRF4-GIF1 gene. Journal of Integrative Plant Biology 63: 2038-2042.
François J, Lallemand M, Fleurat-Lessard P, Laquitaine L, Delrot S, Coutos-Thévenot P, Gomès E. 2008. Overexpression of the VvLTP1 gene interferes with somatic embryo development in grapevine. Functional Plant Biology 35: 394-402.
Guo HH, Guo HX, Zhang L, Fan YJ, Fan YP, Zeng FC. 2019a. SELTP-assembled battery drives totipotency of somatic plant cell. Plant Biotechnology Journal 17: 1188-1190.
Guo HH, Guo HX, Zhang L, Fan YJ, Wu JF, Tang ZM, Zhang Y, Fan YP, Zeng FC. 2020. Dynamic transcriptome analysis reveals uncharacterized complex regulatory pathway underlying genotype-recalcitrant somatic embryogenesis transdifferentiation in cotton. Genes 11: 519.
Guo HH, Wu JF, Chen CX, Wang HM, Zhao YL, Zhang CJ, Jia YH, Liu F, Ning TY, Chu ZH et al. 2019b. Identification and characterization of cell cultures with various embryogenic/regenerative potential in cotton based on morphological, cytochemical, and cytogenetical assessment. Journal of Integrative Agriculture 18: 1-8.
Gupta PK, Durzan DJ. 1987. Biotechnology of somatic polyembryogenesis and plantlet regeneration in loblolly pine. Nature Biotechnology 5: 147-151.
Gutiérrez-Mora A, González-Gutiérrez AG, Rodríguez-Garay B, Ascencio-Cabral A, Li-Wei L. 2012. Plant somatic embryogenesis: some useful considerations. In: Sato K-i, ed. Embryogenesis. London, UK: IntechOpen, 229-248.
Ham BK, Li G, Kang BH, Zeng F, Lucas WJ. 2012. Overexpression of Arabidopsis plasmodesmata germin-like proteins disrupts root growth and development. Plant Cell 24: 3630-3648.
Harada JJ. 1999. Signaling in plant embryogenesis. Current Opinion in Plant Biology 2: 23-27.
Helliwell CA, Wesley SV, Wielopolska AJ, Waterhouse PM. 2002. High-throughput vectors for efficient gene silencing in plants. Functional Plant Biology 29: 1217-1225.
Kamila GJ, Katarzyna KL, Anneke H, Mercedes S, Li M, Karol M, Kim B, Kurczynska EU. 2020. Symplasmic isolation marks cell fate changes during somatic embryogenesis. Journal of Experimental Botany 71: 2612-2628.
Karami O, Philipsen C, Rahimi A, Nurillah AR, Boutilier K, Offringa R. 2023. Endogenous auxin maintains embryonic cell identity and promotes somatic embryo development in Arabidopsis. The Plant Journal 113: 7-22.
Khanday I, Santos-Medellín C, Sundaresan V. 2023. Somatic embryo initiation by rice BABY BOOM1 involves activation of zygote-expressed auxin biosynthesis genes. New Phytologist 238: 673-687.
Kurczynska EU, Potocka I, Dobrowolska I, Kulinskalukaszek K, Sala K, Wrobel J. 2012. Cellular markers for somatic embryogenesis. In: Sato K-I, ed. Embryogenesis. London, UK: IntechOpen, 307-332.
Kwong RW, Bui AQ, Lee H, Kwong LW, Fischer RL, Goldberg RB, Harada JJ. 2003. LEAFY COTYLEDON1-LIKE defines a class of regulators essential for embryo development. Plant Cell 15: 5-18.
Lee HG, Jang SY, Jie EY, Choi SH, Park OS, Bae SH, Kim HS, Kim SW, Hwang GS, Seo PJ. 2023. Adenosine monophosphate enhances callus regeneration competence for de novo plant organogenesis. Molecular Plant 16: 1867-1870.
Li M, Wrobel-Marek J, Heidmann I, Horstman A, Chen B, Reis R, Angenent GC, Boutilier K. 2022. Auxin biosynthesis maintains embryo identity and growth during BABY BOOM-induced somatic embryogenesis. Plant Physiology 188: 1095-1110.
Liu F, Zhang X, Lu C, Zeng X, Li Y, Fu D, Wu G. 2015. Non-specific lipid transfer proteins in plants: presenting new advances and an integrated functional analysis. Journal of Experimental Botany 66: 5663-5681.
Liu J, Tian H, Zhang M, Sun Y, Wang J, Yu Q, Ding Z. 2023. STOP1 attenuates the auxin response to maintain root stem cell niche identity. Cell Reports 43: 113617.
Liu X, Bie XM, Lin X, Li M, Wang H, Zhang X, Yang Y, Zhang C, Zhang XS, Xiao J. 2023. Uncovering the transcriptional regulatory network involved in boosting wheat regeneration and transformation. Nature Plants 9: 908-925.
Liu Z, Dai X, Li J, Liu N, Liu X, Li S, Xiang F. 2020. The type-B cytokinin response regulator ARR1 inhibits shoot regeneration in an ARR12-dependent manner in Arabidopsis. Plant Cell 32: 2271-2291.
Lopes FL, Galvan-Ampudia C, Landrein B. 2021. WUSCHEL in the shoot apical meristem: old player, new tricks. Journal of Experimental Botany 72: 1527-1535.
Lu L, Holt A, Chen X, Liu Y, Knauer S, Tucker EJ, Sarkar AK, Hao Z, Roodbarkelari F, Shi J et al. 2023. miR394 enhances WUSCHEL-induced somatic embryogenesis in Arabidopsis thaliana. New Phytologist 238: 1059-1072.
Lucas WJ, Lee JY. 2004. Plasmodesmata as a supracellular control network in plants. Nature Reviews Molecular Cell Biology 5: 712-726.
Lucau-Danila A, Laborde L, Legrand S, Huot L, Hot D, Lemoine Y, Hilbert JL, Hawkins S, Quillet MC, Hendriks T et al. 2010. Identification of novel genes potentially involved in somatic embryogenesis in chicory (Cichorium intybus L.). BMC Plant Biology 10: 122.
Luo G, Palmgren M. 2021. GRF-GIF chimeras boost plant regeneration. Trends in Plant Science 26: 201-204.
McFarland FL, Collier R, Walter N, Martinell B, Kaeppler SM, Kaeppler HF. 2023. A key to totipotency: Wuschel-like homeobox 2a unlocks embryogenic culture response in maize (Zea mays L.). Plant Biotechnology Journal 21: 1860-1872.
Min L, Hu Q, Li Y, Xu J, Ma Y, Zhu L, Yang X, Zhang X. 2015. LEAFY COTYLEDON1-CASEIN KINASE I-TCP15-PHYTOCHROME INTERACTING FACTOR4 network regulates somatic embryogenesis by regulating auxin homeostasis. Plant Physiology 169: 2805-2821.
Mohanta TK, Yadav D, Khan AL, Hashem A, Abd Allah EF, Al-Harrasi A. 2019. Molecular players of EF-hand containing calcium signaling event in plants. International Journal of Molecular Sciences 20: 1476.
Ogura N, Sasagawa Y, Ito T, Tameshige T, Kawai S, Sano M, Doll Y, Iwase A, Kawamura A, Suzuki T et al. 2023. WUSCHEL-RELATED HOMEOBOX 13 suppresses de novo shoot regeneration via cell fate control of pluripotent callus. Science Advances 9: eadg6983.
Oparka KJ. 2004. Getting the message across: how do plant cells exchange macromolecular complexes? Trends in Plant Science 9: 33-41.
Pedroso MC, Pais MS. 1995. Factors controlling somatic embryogenesis. Plant Cell Tissue and Organ Culture 43: 147-154.
Pina A, Errea P, Schulz A, Martens HJ. 2009. Cell-to-cell transport through plasmodesmata in tree callus cultures. Tree Physiology 29: 809-818.
Poon S, Heath RL, Clarke AE. 2012. A chimeric arabinogalactan protein promotes somatic embryogenesis in cotton cell culture. Plant Physiology 160: 684-695.
Potocka I, Baldwin TC, Kurczynska EU. 2012. Distribution of lipid transfer protein 1 (LTP1) epitopes associated with morphogenic events during somatic embryogenesis of Arabidopsis thaliana. Plant Cell Reports 31: 2031-2045.
Roeder AHK, Otegui MS, Dixit R, Anderson CT, Faulkner C, Zhang Y, Harrison MJ, Kirchhelle C, Goshima G, Coate JE et al. 2022. Fifteen compelling open questions in plant cell biology. Plant Cell 34: 72-102.
Romberger JA, Hejnowicz Z, Hill JF. 2004. Plant structure: function and development. A treatise on anatomy and vegetative development, with special reference to woody plants. Berlin, Germany: Springer-Verlag GmbH & Co. KG.
Ruan YL, Llewellyn DJ, Furbank RT. 2001. The control of single-celled cotton fiber elongation by developmentally reversible gating of plasmodesmata and coordinated expression of sucrose and K+ transporters and expansin. Plant Cell 13: 47-60.
Scheres B. 2001. Plant cell identity. The role of position and lineage. Plant Physiology 125: 112-114.
Sevilem I, Yadav SR, Helariutta Y. 2015. Plasmodesmata: channels for intercellular signaling during plant growth and development. In: Heinlein M, ed. Plasmodesmata. Methods in molecular biology, vol. 1217. New York, NY, USA: Humana Press, 3-24.
Steiner N, Farias-Soares FL, Schmidt ÉC, Pereira ML, Scheid B, Rogge-Renner GD, Bouzon ZL, Schmitz D, Maldonado S, Guerra MP. 2016. Toward establishing a morphological and ultrastructural characterization of proembryogenic masses and early somatic embryos of Araucaria angustifolia (Bert.) O. Kuntze. Protoplasma 253: 487-501.
Steinmacher DA, Guerra MP, Saare-Surminski K, Lieberei R. 2011. A temporary immersion system improves in vitro regeneration of peach palm through secondary somatic embryogenesis. Annals of Botany 108: 1463-1475.
Sterk P, Booij H, Schellekens GA, Van Kammen A, De Vries SC. 1991. Cell-specific expression of the carrot EP2 lipid transfer protein gene. Plant Cell 3: 907-921.
Tian W, Hou C, Ren Z, Wang C, Zhao F, Dahlbeck D, Hu S, Zhang L, Niu Q, Li L et al. 2019. A calmodulin-gated calcium channel links pathogen patterns to plant immunity. Nature 572: 131-135.
Verdeil JL, Alemanno L, Niemenak N, Tranbarger TJ. 2007. Pluripotent versus totipotent plant stem cells: dependence versus autonomy? Trends in Plant Science 12: 245-252.
Vogel G. 2005. How does a single somatic cell become a whole plant? Science 309: 86.
Walter M, Chaban C, Schütze K, Batistic O, Weckermann K, Näke C, Blazevic D, Grefen C, Schumacher K, Oecking C et al. 2004. Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. The Plant Journal 40: 428-438.
Wang H, Sun Y, Chang J, Zheng F, Pei H, Yi Y, Chang C, Dong CH. 2016. Regulatory function of Arabidopsis lipid transfer protein 1 (LTP1) in ethylene response and signaling. Plant Molecular Biology 91: 471-484.
Wang K, Shi L, Liang X, Zhao P, Wang W, Liu J, Chang Y, Hiei Y, Yanagihara C, Du L et al. 2022. The gene TaWOX5 overcomes genotype dependency in wheat genetic transformation. Nature Plants 8: 110-117.
Wang N, Ryan L, Sardesai N, Wu E, Lenderts B, Lowe K, Che P, Anand A, Worden A, van Dyk D et al. 2023. Leaf transformation for efficient random integration and targeted genome modification in maize and sorghum. Nature Plants 9: 255-270.
Wang P, Duckney P, Gao E, Hussey PJ, Kriechbaumer V, Li C, Zang J, Zhang T. 2023. Keep in contact: multiple roles of endoplasmic reticulum-membrane contact sites and the organelle interaction network in plants. New Phytologist 238: 482-499.
Wang P, Hawes C, Hussey PJ. 2017. Plant endoplasmic reticulum-plasma membrane contact sites. Trends in Plant Science 22: 289-297.
Wang X, Niu QW, Teng C, Li C, Mu J, Chua NH, Zuo J. 2009. Overexpression of PGA37/MYB118 and MYB115 promotes vegetative-to-embryonic transition in Arabidopsis. Cell Research 19: 224-235.
Wu J, Chang X, Li C, Zhang Z, Zhang J, Yin C, Ma W, Chen H, Zhou F, Lin Y. 2022. QTLs related to rice callus regeneration ability: localization and effect verification of qPRR3. Cells 11: 4125.
Wu LY, Shang GD, Wang FX, Gao J, Wan MC, Xu ZG, Wang JW. 2022. Dynamic chromatin state profiling reveals regulatory roles of auxin and cytokinin in shoot regeneration. Developmental Cell 57: 526-542.
Xu C, Chang P, Guo S, Yang X, Liu X, Sui B, Yu D, Xin W, Hu Y. 2023. Transcriptional activation by WRKY23 and derepression by removal of bHLH041 coordinately establish callus pluripotency in Arabidopsis regeneration. Plant Cell 36: 158-173.
Xu M, Du Q, Tian C, Wang Y, Jiao Y. 2021. Stochastic gene expression drives mesophyll protoplast regeneration. Science Advances 7: eabg8466.
Yang Z, Liu Z, Ge X, Lu L, Qin W, Qanmber G, Liu L, Wang Z, Li F. 2023. Brassinosteroids regulate cotton fiber elongation by modulating very-long-chain fatty acid biosynthesis. Plant Cell 35: 2114-2131.
Yao Y, Xiang D, Wu N, Wang Y, Chen Y, Yuan Y, Ye Y, Hu D, Zheng C, Yan Y et al. 2023. Control of rice ratooning ability by a nucleoredoxin that inhibits histidine kinase dimerization to attenuate cytokinin signaling in axillary buds. Molecular Plant 16: 1911-1926.
Yu Y, Yu H, Peng J, Yao WJ, Wang YP, Zhang FL, Wang SR, Zhao Y, Zhao XY, Zhang XS et al. 2023. Enhancing wheat regeneration and genetic transformation through overexpression of TaLAX1. Plant Communications 5: 100738.
Yuan J, Liu X, Zhao H, Wang Y, Wei X, Wang P, Zhan J, Liu L, Li F, Ge X. 2023. GhRCD1 regulates cotton somatic embryogenesis by modulating the GhMYC3-GhMYB44-GhLBD18 transcriptional cascade. New Phytologist 240: 207-223.
Zeng F, Zhang X, Zhu L, Tu L, Guo X, Nie Y. 2006. Isolation and characterization of genes associated to cotton somatic embryogenesis by suppression subtractive hybridization and macroarray. Plant Molecular Biology 60: 167-183.
Zhai N, Xu L. 2021. Pluripotency acquisition in the middle cell layer of callus is required for organ regeneration. Nature Plants 7: 1453-1460.
Zhang G, Zhao F, Chen L, Pan Y, Sun L, Bao N, Zhang T, Cui CX, Qiu Z, Zhang Y et al. 2019. Jasmonate-mediated wound signalling promotes plant regeneration. Nature Plants 5: 491-497.
Zhang S, Yu R, Yu D, Chang P, Guo S, Yang X, Liu X, Xu C, Hu Y. 2022. The calcium signaling module CaM-IQM destabilizes IAA-ARF interaction to regulate callus and lateral root formation. Proceedings of the National Academy of Sciences, USA 119: e2202669119.
Zhang TQ, Lian H, Zhou CM, Xu L, Jiao Y, Wang JW. 2017. A two-step model for de novo activation of WUSCHEL during plant shoot regeneration. Plant Cell 29: 1073-1087.
Zhang Y, Cai G, Zhang K, Sun H, Huang L, Ren W, Ding Y, Wang N. 2024. PdeERF114 recruits PdeWRKY75 to regulate callus formation in poplar by modulating the accumulation of H2O2 and the relaxation of cell walls. New Phytologist 241: 732-746.
Zhang YC, Zhou YF, Cheng Y, Huang JH, Lian JP, Yang L, He RR, Lei MQ, Liu YW, Yuan C et al. 2022. Genome-wide analysis and functional annotation of chromatin-enriched noncoding RNAs in rice during somatic cell regeneration. Genome Biology 23: 28.
Zhou W, Lozano-Torres JL, Blilou I, Zhang X, Zhai Q, Smant G, Li C, Scheres B. 2019. A jasmonate signaling network activates root stem cells and promotes regeneration. Cell 177: 942-956.