How alternative splicing changes the properties of plant proteins
Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic-ecollection
Typ dokumentu časopisecké články, přehledy
PubMed
37077961
PubMed Central
PMC10095807
DOI
10.1017/qpb.2022.9
PII: S2632882822000091
Knihovny.cz E-zdroje
- Klíčová slova
- RNA processing, alternative splicing, competitive inhibition, feedback loop, network motifs, plant development,
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
Most plant primary transcripts undergo alternative splicing (AS), and its impact on protein diversity is a subject of intensive investigation. Several studies have uncovered various mechanisms of how particular protein splice isoforms operate. However, the common principles behind the AS effects on protein function in plants have rarely been surveyed. Here, on the selected examples, we highlight diverse tissue expression patterns, subcellular localization, enzymatic activities, abilities to bind other molecules and other relevant features. We describe how the protein isoforms mutually interact to underline their intriguing roles in altering the functionality of protein complexes. Moreover, we also discuss the known cases when these interactions have been placed inside the autoregulatory loops. This review is particularly intended for plant cell and developmental biologists who would like to gain inspiration on how the splice variants encoded by their genes of interest may coordinately work.
Zobrazit více v PubMed
Abascal, F. , Ezkurdia, I. , Rodriguez-Rivas, J. , Rodriguez, J. M. , del Pozo, A. , Vázquez, J. , Valencia, A. , & Tress, M. L . (2015). Alternatively spliced homologous exons have ancient origins and are highly expressed at the protein level. PLOS Computational Biology, 11, e1004325. PubMed PMC
Airoldi, C. A. , McKay, M. , & Davies, B. (2015). MAF2 is regulated by temperature-dependent splicing and represses flowering at low temperatures in parallel with FLM. PLoS One, 10, e0126516. PubMed PMC
Alon, U. (2007). Network motifs: Theory and experimental approaches. Nature Reviews Genetics, 8, 450–461. PubMed
Blencowe, B. J. (2017). The relationship between alternative splicing and proteomic complexity. Trends in Biochemical Sciences, 42, 407–408. PubMed
Brown, J. W. S. , Simpson, C. G. , Marquez, Y. , Gadd, G. M. , Barta, A. , & Kalyna, M. (2015). Lost in translation: Pitfalls in deciphering plant alternative splicing transcripts. The Plant Cell, 27, 2083–2087. PubMed PMC
Capovilla, G. , Symeonidi, E. , Wu, R. , & Schmid, M. (2017). Contribution of major FLM isoforms to temperature-dependent flowering in Arabidopsis thaliana. Journal of Experimental Botany, 68, 5117–5127. PubMed PMC
Carqueijeiro, I. , Koudounas, K. , Dugé de Bernonville, T. , Sepúlveda, LJ. , Mosquera, A. , Bomzan, DP. , Oudin, A. , Lanoue, A. , Besseau, S. , Lemos Cruz, P. , Kulagina, N. , Stander, EA. , Eymieux, S. , Burlaud-Gaillard, J. , Blanchard, E. , Clastre, M. , Atehortùa, L. , St-Pierre, B. , Giglioli-Guivarc'h, N. , Papon, N. , Nagegowda, DA. , O'Connor, SE. , Courdavault, V. (2021). Alternative splicing creates a pseudo-strictosidine β-d-glucosidase modulating alkaloid synthesis in Catharanthus roseus. Plant Physiology, 185, 836–856. PubMed PMC
Carvalho, R. F. , Feijão, C. V. , & Duque, P. (2013). On the physiological significance of alternative splicing events in higher plants. Protoplasma, 250, 639–650. PubMed
Chaudhary, S. , Jabre, I. , Reddy, A. S. N. , Staiger, D. , & Syed, N. H. (2019a). Perspective on alternative splicing and proteome complexity in plants. Trends in Plant Science, 24, 496–506. PubMed
Chaudhary, S. , Khokhar, W. , Jabre, I. , Reddy, A. S. N. , Byrne, L. J. , Wilson, C. M. , & Syed, N. H. (2019b). Alternative splicing and protein diversity: Plants versus animals. Frontiers in Plant Science, 10, 708. PubMed PMC
Chung, H. S. , & Howe, G. A. (2009). A critical role for the TIFY motif in repression of Jasmonate signaling by a stabilized splice variant of the JASMONATE ZIM-domain protein JAZ10 in Arabidopsis . The Plant Cell, 21, 131–145. PubMed PMC
Cucinotta, M. , Cavalleri, A. , Guazzotti, A. , Astori, C. , Manrique, S. , Bombarely, A. , Oliveto, S. , Biffo, S. , Weijers, D. , Kater, M. M. , Colombo, L. (2021). Alternative splicing generates a MONOPTEROS isoform required for ovule development. Current Biology, 31, 892–899.e3. PubMed
Cyrek, M. , Fedak, H. , Ciesielski, A. , Guo, Y. , Sliwa, A. , Brzezniak, L. , Krzyczmonik, K. , Pietras, Z. , Kaczanowski, S. , Liu, F. , et al. (2016). Seed dormancy in Arabidopsis is controlled by alternative polyadenylation of DOG1 . Plant Physiology, 170, 947–955. PubMed PMC
Dressano, K. , Weckwerth, P. R. , Poretsky, E. , Takahashi, Y. , Villarreal, C. , Shen, Z. , Schroeder, J. I. , Briggs, S. P. , & Huffaker, A. (2020). Dynamic regulation of pep-induced immunity through post-translational control of defence transcript splicing. Nature Plants, 6, 1008–1019. PubMed PMC
Filichkin, S. , Priest, H. D. , Megraw, M. , & Mockler, T. C. (2015). Alternative splicing in plants: Directing traffic at the crossroads of adaptation and environmental stress. Current Opinion in Plant Biology, 24, 125–135. PubMed
Fonouni-Farde, C. , Ariel, F. , & Crespi, M. (2021). Plant long noncoding RNAs: New players in the field of post-transcriptional regulations. Non-Coding RNA, 7, 12. PubMed PMC
Ghelli, R. , Brunetti, P. , Napoli, N. , De Paolis, A. , Cecchetti, V. , Tsuge, T. , Serino, G. , Matsui, M. , Mele, G. , Rinaldi, G. , Palumbo, GA. , Barozzi, F. , Costantino, P. , Cardarelli, M. (2018). A newly identified flower-specific splice variant of AUXIN RESPONSE FACTOR8 regulates stamen elongation and endothecium lignification in Arabidopsis. The Plant Cell, 30, 620–637. PubMed PMC
Gil, K.-E. , Park, M.-J. , Lee, H.-J. , Park, Y.-J. , Han, S.-H. , Kwon, Y.-J. , Seo, P. J. , Jung, J.-H. , & Park, C.-M. (2017). Alternative splicing provides a proactive mechanism for the diurnal CONSTANS dynamics in Arabidopsis photoperiodic flowering. The Plant Journal, 89, 128–140. PubMed
Hartmann, L. , Wießner, T. , & Wachter, A. (2018). Subcellular compartmentation of alternatively spliced transcripts defines SERINE/ARGININE-RICH PROTEIN30 expression. Plant Physiology, 176, 2886–2903. PubMed PMC
Howe, G. A. , Major, I. T. , & Koo, A. J. (2018). Modularity in Jasmonate signaling for multistress resilience. Annual Review of Plant Biology, 69, 387–415. PubMed
Hrtyan, M. , Šliková, E. , Hejátko, J. , & Růžička, K. (2015). RNA processing in auxin and cytokinin pathways. Journal of Experimental Botany, 66, 4897–4912. PubMed
Hu, Y. , Mesihovic, A. , Jiménez‐Gómez, J. M. , Röth, S. , Gebhardt, P. , Bublak, D. , Bovy, A. , Scharf, K. , Schleiff, E. , & Fragkostefanakis, S. (2020). Natural variation in HsfA2 pre‐mRNA splicing is associated with changes in thermotolerance during tomato domestication. New Phytologist, 225, 1297–1310. PubMed
Huang, C.-K. , Lin, W.-D. , & Wu, S.-H. (2022). An improved repertoire of splicing variants and their potential roles in Arabidopsis photomorphogenic development. Genome Biology, 23, 50. PubMed PMC
Jangi, M. , & Sharp, P. A. (2014). Building robust transcriptomes with master splicing factors. Cell, 159, 487–498. PubMed PMC
Jiang, J. , Zhang, C. , & Wang, X. (2015). A recently evolved isoform of the transcription factor BES1 promotes Brassinosteroid signaling and development in Arabidopsis thaliana . The Plant Cell, 27, 361–374. PubMed PMC
Jiao, Y. , & Meyerowitz, E. M. (2010). Cell‐type specific analysis of translating RNAs in developing flowers reveals new levels of control. Molecular Systems Biology, 6, 419. PubMed PMC
Job, N. , Yadukrishnan, P. , Bursch, K. , Datta, S. , & Johansson, H. (2018). Two B-box proteins regulate Photomorphogenesis by oppositely modulating HY5 through their diverse C-terminal domains. Plant Physiology, 176, 2963–2976. PubMed PMC
John, S. , Olas, J. J. , & Mueller-Roeber, B. (2021). Regulation of alternative splicing in response to temperature variation in plants. Journal of Experimental Botany, 72, 6150–6163. PubMed PMC
Kanno, T. , Venhuizen, P. , Wen, T.-N. , Lin, W.-D. , Chiou, P. , Kalyna, M. , Matzke, A. J. M. , & Matzke, M. (2018). PRP4KA, a putative spliceosomal protein kinase, is important for alternative splicing and development in Arabidopsis thaliana . Genetics, 210, 1267–1285. PubMed PMC
Kashkan, I. , Hrtyan, M. , Retzer, K. , Humpolíčková, J. , Jayasree, A. , Filepová, R. , Vondráková, Z. , Simon, S. , Rombaut, D. , Jacobs, T. B. , Frilander, M. J. , Hejátko, J. , Friml, J. , Petrášek, J. , & Růžička, K. (2021). Mutually opposing activity of PIN7 splicing isoforms is required for auxin‐mediated tropic responses in Arabidopsis thaliana. New Phytologist, 233, 329–343. PubMed
Kashkan, I. , Timofeyenko, K. , Kollárová, E. , & Růžička, K. (2020). In vivo reporters for visualizing alternative splicing of hormonal genes. Plants, 9, 868. PubMed PMC
Kelemen, O. , Convertini, P. , Zhang, Z. , Wen, Y. , Shen, M. , Falaleeva, M. , & Stamm, S. (2013). Function of alternative splicing. Gene, 514, 1–30. PubMed PMC
Kim, J. , Ryu, J. Y. , Baek, K. , & Park, C. (2016). High temperature attenuates the gravitropism of inflorescence stems by inducing SHOOT GRAVITROPISM 5 alternative splicing in Arabidopsis rabidopsis . New Phytologist, 209, 265–279. PubMed
Klepikova, A. V. , Kasianov, A. S. , Gerasimov, E. S. , Logacheva, M. D. , & Penin, A. A. (2016). A high resolution map of the Arabidopsis thaliana developmental transcriptome based on RNA-seq profiling. The Plant Journal, 88, 1058–1070. PubMed
Kriechbaumer, V. , Botchway, S. W. , & Hawes, C. (2017). Localization and interactions between Arabidopsis auxin biosynthetic enzymes in the TAA/YUC-dependent pathway. Journal of Experimental Botany, 68, 4195–4207. PubMed
Kriechbaumer, V. , Wang, P. , Hawes, C. , & Abell, B. M. (2012). Alternative splicing of the auxin biosynthesis gene YUCCA4 determines its subcellular compartmentation: YUCCA4 and auxin biosynthesis. The Plant Journal, 70, 292–302. PubMed
Lamberto, I. , Percudani, R. , Gatti, R. , Folli, C. , & Petrucco, S. (2010). Conserved alternative splicing of Arabidopsis transthyretin-like determines protein localization and S-Allantoin synthesis in peroxisomes. The Plant Cell, 22, 1564–1574. PubMed PMC
Lee, T. I. , Rinaldi, N. J. , Robert, F. , Odom, D. T. , Bar-Joseph, Z. , Gerber, G. K. , Hannett, N. M. , Harbison, C. T. , Thompson, C. M. , Simon, I. , Zeitlinger, J. , Jennings, E. G. , Murray, H. L. , Gordon, D. B. , Ren, B. , Wyrick, J. J. , Tagne, J. B. , Volkert, T. L. , Fraenkel, E. , Gifford, D. K. , Young, R. A. 2002. Transcriptional regulatory networks in saccharomyces cerevisiae. Science, 298, 799–804. PubMed
Lee, Y. , & Rio, D. C. (2015). Mechanisms and regulation of alternative pre-mRNA splicing. Annual Review of Biochemistry, 84, 291–323. PubMed PMC
Lee, J. H. , Ryu, H.-S. , Chung, K. S. , Pose, D. , Kim, S. , Schmid, M. , & Ahn, J. H. (2013). Regulation of temperature-responsive flowering by MADS-box transcription factor repressors. Science, 342, 628–632. PubMed
Li, Z. , Tang, J. , Bassham, D. C. , & Howell, S. H. (2021). Daily temperature cycles promote alternative splicing of RNAs encoding SR45a, a splicing regulator in maize. Plant Physiology, 186, 1318–1335. PubMed PMC
Li, S. , Yamada, M. , Han, X. , Ohler, U. , & Benfey, P. N. (2016). High-resolution expression map of the Arabidopsis root reveals alternative splicing and lincRNA regulation. Developmental Cell, 39, 508–522. PubMed PMC
Lin, W.-Y. , Matsuoka, D. , Sasayama, D. , & Nanmori, T. (2010). A splice variant of Arabidopsis mitogen-activated protein kinase and its regulatory function in the MKK6–MPK13 pathway. Plant Science, 178, 245–250.
Liu, J. , Sun, N. , Liu, M. , Liu, J. , Du, B. , Wang, X. , & Qi, X. (2013). An autoregulatory loop controlling Arabidopsis HsfA2 expression: Role of heat shock-induced alternative splicing. Plant Physiology, 162, 512–521. PubMed PMC
Lutz, U. , Nussbaumer, T. , Spannagl, M. , Diener, J. , Mayer, K. F. , & Schwechheimer, C. (2017). Natural haplotypes of FLM non-coding sequences fine-tune flowering time in ambient spring temperatures in Arabidopsis. eLife, 6, e22114. PubMed PMC
Lutz, U. , Posé, D. , Pfeifer, M. , Gundlach, H. , Hagmann, J. , Wang, C. , Weigel, D. , Mayer, K. F. X. , Schmid, M. , & Schwechheimer, C. (2015). Modulation of ambient temperature-dependent flowering in Arabidopsis thaliana by natural variation of FLOWERING LOCUS M. PLoS Genetics, 11, e1005588. PubMed PMC
Marquez, Y. , Brown, J. W. S. , Simpson, C. , Barta, A. , & Kalyna, M. (2012). Transcriptome survey reveals increased complexity of the alternative splicing landscape in Arabidopsis . Genome Research, 22, 1184–1195. PubMed PMC
Marquez, Y. , Höpfler, M. , Ayatollahi, Z. , Barta, A. , & Kalyna, M. (2015). Unmasking alternative splicing inside protein-coding exons defines exitrons and their role in proteome plasticity. Genome Research, 25, 995–1007. PubMed PMC
Martín, G. , Márquez, Y. , Mantica, F. , Duque, P. , & Irimia, M. (2021). Alternative splicing landscapes in Arabidopsis thaliana across tissues and stress conditions highlight major functional differences with animals. Genome Biology, 22, 35. PubMed PMC
Moreno, J. E. , Shyu, C. , Campos, M. L. , Patel, L. C. , Chung, H. S. , Yao, J. , He, S. Y. , & Howe, G. A. (2013). Negative feedback control of jasmonate signaling by an alternative splice variant of JAZ10. Plant Physiology, 162, 1006–1017. PubMed PMC
Nagarajan, R. , & Gill, K. S. (2018). Evolution of rubisco activase gene in plants. Plant Molecular Biology, 96, 69–87. PubMed
Nakabayashi, K. , Bartsch, M. , Ding, J. , & Soppe, W. J. J . (2015). Seed dormancy in Arabidopsis requires self-Binding ability of DOG1 protein and the presence of multiple isoforms generated by alternative splicing. PLoS Genetics, 11, e1005737. PubMed PMC
Nicolas, M. , Rodríguez-Buey, M. L. , Franco-Zorrilla, J. M. , & Cubas, P. (2015). A recently evolved alternative splice site in the BRANCHED1a gene controls potato plant architecture. Current Biology, 25, 1799–1809. PubMed
Posé, D. , Verhage, L. , Ott, F. , Yant, L. , Mathieu, J. , Angenent, G. C. , Immink, R. G. H. , & Schmid, M. (2013). Temperature-dependent regulation of flowering by antagonistic FLM variants. Nature, 503, 414–417. PubMed
Quesada, V. , Macknight, R. , Dean, C. , & Simpson, G. G . (2003) Autoregulation of FCA pre-mRNA processing controls Arabidopsis owering time. The EMBO Journal, 22, 3142–3152. PubMed PMC
Reddy, A. S. N. , Marquez, Y. , Kalyna, M. , & Barta, A. (2013). Complexity of the alternative splicing landscape in plants. The Plant Cell, 25, 3657–3683. PubMed PMC
Reixachs-Solé, M. , Ruiz-Orera, J. , Albà, M. M. , & Eyras, E. (2020). Ribosome profiling at isoform level reveals evolutionary conserved impacts of differential splicing on the proteome. Nature Communications, 11, 1768. PubMed PMC
Remy, E. , Cabrito, T. R. , Baster, P. , Batista, R. A. , Teixeira, M. C. , Friml, J. , Sá-Correia, I. , & Duque, P. (2013). A major facilitator superfamily transporter plays a dual role in polar auxin transport and drought stress tolerance in Arabidopsis . The Plant Cell, 25, 901–926. PubMed PMC
Rodriguez, J. M. , Pozo, F. , di Domenico, T. , Vazquez, J. , & Tress, M. L . (2020). An analysis of tissue-specific alternative splicing at the protein level. PLoS Computational Biology, 16, e1008287. PubMed PMC
Samach, A. , Melamed-Bessudo, C. , Avivi-Ragolski, N. , Pietrokovski, S. , & Levy, A. A. (2011). Identification of plant RAD52 homologs and characterization of the Arabidopsis thaliana RAD52 -like genes. The Plant Cell, 23, 4266–4279. PubMed PMC
Schöning, J. C. , Streitner, C. , Meyer, I. M. , Gao, Y. , & Staiger, D. (2008). Reciprocal regulation of glycine-rich RNA-binding proteins via an interlocked feedback loop coupling alternative splicing to nonsense-mediated decay in Arabidopsis. Nucleic Acids Research, 36, 6977–6987. PubMed PMC
Seo, P. J. , Hong, S.-Y. , Kim, S.-G. , & Park, C.-M. (2011a). Competitive inhibition of transcription factors by small interfering peptides. Trends in Plant Science, 16, 541–549. PubMed
Seo, P. J. , Kim, M. J. , Ryu, J.-Y. , Jeong, E.-Y. , & Park, C.-M. (2011b). Two splice variants of the IDD14 transcription factor competitively form nonfunctional heterodimers which may regulate starch metabolism. Nature Communications, 2, 303. PubMed
Seo, P. J. , Park, M.-J. , Lim, M.-H. , Kim, S.-G. , Lee, M. , Baldwin, I. T. , & Park, C.-M. (2012). A self-regulatory circuit of CIRCADIAN CLOCK-ASSOCIATED1 underlies the circadian clock regulation of temperature responses in Arabidopsis . The Plant Cell, 24, 2427–2442. PubMed PMC
Shang, X. , Cao, Y. , & Ma, L. (2017). Alternative splicing in plant genes: A means of regulating the environmental fitness of plants. International Journal of Molecular Sciences, 18, 432. PubMed PMC
Shen, J. B. , Orozco, E. M. , & Ogren, W. L. (1991). Expression of the two isoforms of spinach ribulose 1,5-bisphosphate carboxylase activase and essentiality of the conserved lysine in the consensus nucleotide-binding domain. Journal of Biological Chemistry, 266, 8963–8968. PubMed
Shikata, H. , Hanada, K. , Ushijima, T. , Nakashima, M. , Suzuki, Y. , & Matsushita, T. (2014). Phytochrome controls alternative splicing to mediate light responses in Arabidopsis . Proceedings of the National Academy of Sciences, 111, 18781–18786. PubMed PMC
Staiger, D. , & Brown, J. W. S. (2013). Alternative splicing at the intersection of biological timing, development, and stress responses. The Plant Cell, 25, 3640–3656. PubMed PMC
Stamm, S. , Ben-Ari, S. , Rafalska, I. , Tang, Y. , Zhang, Z. , Toiber, D. , Thanaraj, T. A. , & Soreq, H. (2005). Function of alternative splicing. Gene, 344, 1–20. PubMed
Sugio, A. , Dreos, R. , Aparicio, F. , & Maule, A. J. (2009). The cytosolic protein response as a subcomponent of the wider heat shock response in Arabidopsis . The Plant Cell, 21, 642–654. PubMed PMC
Sureshkumar, S. , Dent, C. , Seleznev, A. , Tasset, C. , & Balasubramanian, S. (2016). Nonsense-mediated mRNA decay modulates FLM-dependent thermosensory flowering response in Arabidopsis. Nature Plants, 2, 16055. PubMed
Szakonyi, D. , & Duque, P. (2018). Alternative splicing as a regulator of early plant development. Frontiers in Plant Science, 9, 1174. PubMed PMC
Szécsi, J. , Joly, C. , Bordji, K. , Varaud, E. , Cock, J. M. , Dumas, C. , & Bendahmane, M. (2006). BIGPETALp, a bHLH transcription factor is involved in the control ofArabidopsis petal size. EMBO Journal, 25, 3912–3920. PubMed PMC
Tress, M. L. , Abascal, F. , & Valencia, A. (2017a). Alternative splicing may not be the key to proteome complexity. Trends in Biochemical Sciences, 42, 98–110. PubMed PMC
Tress, M. L. , Abascal, F. , & Valencia, A. (2017b). Most alternative isoforms are not functionally important. Trends in Biochemical Sciences, 42, 408–410. PubMed PMC
Varaud, E. , Brioudes, F. , Szécsi, J. , Leroux, J. , Brown, S. , Perrot-Rechenmann, C. , & Bendahmane, M. (2011). AUXIN RESPONSE FACTOR8 regulates Arabidopsis petal growth by interacting with the bHLH transcription FACTOR BIGPETALp. The Plant Cell, 23, 973–983. PubMed PMC
Wang, Z. , & Burge, C. B. (2008). Splicing regulation: From a parts list of regulatory elements to an integrated splicing code. RNA, 14, 802–813. PubMed PMC
Wang, Z. , Ji, H. , Yuan, B. , Wang, S. , Su, C. , Yao, B. , Zhao, H. , & Li, X. (2015). ABA signalling is fine-tuned by antagonistic HAB1 variants. Nature Communications, 6, 8138. PubMed
Weatheritt, R. J. , Sterne-Weiler, T. , & Blencowe, B. J. (2016). The ribosome-engaged landscape of alternative splicing. Nature Structural & Molecular Biology, 23, 1117–1123. PubMed PMC
Werneke, J. M. , Chatfield, J. M. , & Ogren, W. L . (1989) Alternative mRNA splicing generates the two ribulosebisphosphate carboxylase/oxygenase activase polypeptides in spinach and Arabídopsis. 1, 815–825. PubMed PMC
Wu, F. , Deng, L. , Zhai, Q. , Zhao, J. , Chen, Q. , & Li, C. (2020). Mediator subunit MED25 couples alternative splicing of JAZ genes with fine-tuning of Jasmonate signaling. The Plant Cell, 32, 429–448. PubMed PMC
Yan, Y. , Stolz, S. , Chételat, A. , Reymond, P. , Pagni, M. , Dubugnon, L. , & Farmer, E. E. (2007). A downstream mediator in the growth repression limb of the jasmonate pathway. The Plant Cell, 19, 2470–2483. PubMed PMC
Yang, X. , Coulombe-Huntington, J. , Kang, S. , Sheynkman, G. M. , Hao, T. , Richardson, A. , Sun, S. , Yang, F. , Shen, Y. A. , Murray, R. R. , Spirohn, K. , Begg, B. E. , Duran-Frigola, M. , MacWilliams, A. , Pevzner, S. J. , Zhong, Q. , Trigg, S. A. , Tam, S. , Ghamsari, L. , Sahni, N. , Vidal, M. (2016). Widespread expansion of protein interaction capabilities by alternative splicing. Cell, 164, 805–817. PubMed PMC
Yu, H. , Tian, C. , Yu, Y. , & Jiao, Y. (2016). Transcriptome survey of the contribution of alternative splicing to proteome diversity in Arabidopsis thaliana. Molecular Plant, 9, 749–752. PubMed
Zhan, X. , Qian, B. , Cao, F. , Wu, W. , Yang, L. , Guan, Q. , Gu, X. , Wang, P. , Okusolubo, T. A. , Dunn, S. L. , Zhu J.-K., & Zhu, J. (2015). An Arabidopsis PWI and RRM motif-containing protein is critical for pre-mRNA splicing and ABA responses. Nature Communications, 6, 8139. PubMed PMC
Zhang, N. , Kallis, R. P. , Ewy, R. G. , & Portis, A. R. (2002). Light modulation of rubisco in Arabidopsis requires a capacity for redox regulation of the larger rubisco activase isoform. Proceedings of the National Academy of Sciences, 99, 3330–3334. PubMed PMC
Zhang, F. , Ke, J. , Zhang, L. , Chen, R. , Sugimoto, K. , Howe, G. A. , Xu, H. E. , Zhou, M. , He, S. Y. , & Melcher, K. (2017). Structural insights into alternative splicing-mediated desensitization of jasmonate signaling. Proceedings of the National Academy of Sciences, 114, 1720–1725. PubMed PMC
Zhang, S. , Liu, H. , Yuan, L. , Li, X. , Wang, L. , Xu, X. , & Xie, Q. (2021). Recognition of CCA1 alternative protein isoforms during temperature acclimation. Plant Cell Reports, 40, 421–432. PubMed
Zhang, R. , Min, Y. , Holappa, L. D. , Walcher‐Chevillet, C. L. , Duan, X. , Donaldson, E. , Kong, H. , & Kramer, E. M. (2020). A role for the auxin response factors ARF6 and ARF8 homologs in petal spur elongation and nectary maturation in aquilegia . New Phytologist, 227, 1392–1405. PubMed
Zhang, X.-N. , Mo, C. , Garrett, W. M. , & Cooper, B. (2014). Phosphothreonine 218 is required for the function of SR45.1 in regulating flower petal development in Arabidopsis . Plant Signaling & Behavior, 9, e29134. PubMed PMC
Zhang, X.-N. , & Mount, S. M. (2009). Two alternatively spliced isoforms of the Arabidopsis SR45 protein have distinct roles during normal plant development. Plant Physiology, 150, 1450–1458. PubMed PMC
Zhang, N. , & Portis, A. R. (1999). Mechanism of light regulation of rubisco: A specific role for the larger rubisco activase isoform involving reductive activation by thioredoxin-f. Proceedings of the National Academy of Sciences, 96, 9438–9443. PubMed PMC
Zhu, F.-Y. , Chen, M.-X. , Ye, N.-H. , Shi, L. , Ma, K.-L. , Yang, J.-F. , Cao, Y.-Y. , Zhang, Y. , Yoshida, T. , Fernie, A. R. , Fan, G. Y. , Wen, B. , Zhou, R. , Liu, T. Y. , Fan, T. , Gao, B. , Zhang, D. , Hao, G. F. , Xiao, S. , Liu, Y. G. , Zhang, J. (2017). Proteogenomic analysis reveals alternative splicing and translation as part of the abscisic acid response in Arabidopsis seedlings. The Plant Journal, 91, 518–533. PubMed