Isopentenyltransferase-1 (IPT1) knockout in Physcomitrella together with phylogenetic analyses of IPTs provide insights into evolution of plant cytokinin biosynthesis

Lindner, Ann-Cathrin; Lang, Daniel; Seifert, Maike; Podlešáková, Kateřina; Novák, Ondřej; Strnad, Miroslav; Reski, Ralf; Schwartzenberg, Klaus von

doi:10.1093/jxb/eru142

Cited by 55 publications

(64 citation statements)

References 71 publications

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“…Nevertheless, the iP-type and tZ-type cytokinins are still present and are also the most active forms in this moss (28). In a recent study, it was also suggested that a tRNA-independent pathway exists in case of P. patens (29). Therefore, it may be that the nematode tRNA-IPT enzyme catalyzes the production of a broader range of cytokinins.…”

Section: Discussionmentioning

confidence: 90%

A parasitic nematode releases cytokinin that controls cell division and orchestrates feeding site formation in host plants

Siddique

Radakovic

Torre

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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125

118

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Sedentary plant-parasitic cyst nematodes are biotrophs that cause significant losses in agriculture. Parasitism is based on modifications of host root cells that lead to the formation of a hypermetabolic feeding site (a syncytium) from which nematodes withdraw nutrients. The host cell cycle is activated in an initial cell selected by the nematode for feeding, followed by activation of neighboring cells and subsequent expansion of feeding site through fusion of hundreds of cells. It is generally assumed that nematodes manipulate production and signaling of the plant hormone cytokinin to activate cell division. In fact, nematodes have been shown to produce cytokinin in vitro; however, whether the hormone is secreted into host plants and plays a role in parasitism remained unknown. Here, we analyzed the spatiotemporal activation of cytokinin signaling during interaction between the cyst nematode, Heterodera schachtii, and Arabidopsis using cytokinin-responsive promoter:reporter lines. Our results showed that cytokinin signaling is activated not only in the syncytium but also in neighboring cells to be incorporated into syncytium. An analysis of nematode infection on mutants that are deficient in cytokinin or cytokinin signaling revealed a significant decrease in susceptibility of these plants to nematodes. Further, we identified a cytokinin-synthesizing isopentenyltransferase gene in H. schachtii and show that silencing of this gene in nematodes leads to a significant decrease in virulence due to a reduced expansion of feeding sites. Our findings demonstrate the ability of a plant-parasitic nematode to synthesize a functional plant hormone to manipulate the host system and establish a long-term parasitic interaction.Arabidopsis thaliana | cell cycle | cytokinin | cyst nematode | IPT P lant-parasitic nematodes are a significant threat to almost all economically important crops. International surveys revealed an average annual crop yield loss of more than 10% due to nematode infestation and up to 20% for certain crops, e.g., bananas (1). Most of this damage is caused by the sedentary rootknot (Meloidogyne spp.) and cyst nematodes (Globodera spp. and Heterodera spp.). Infective second-stage juveniles (J2) of both rootknot nematodes (RKNs) and cyst nematodes invade plant roots near the tip and move toward the vascular cylinder. On reaching the vascular cylinder, RKNs induce the formation of several giant cells, whereas cyst nematodes induce the formation of a syncytium. These feeding sites serve as the nematode's sole source of nutrients throughout its life cycle for several weeks. Cyst nematodes are dimorphic, but the mechanism of sex determination is not clearly understood. It has, nonetheless, been observed that the environment strongly influences the outcome of the sex ratio in cyst nematodes. Under favorable conditions with plenty of nutrients, the majority of juveniles develop into females. However, when the juveniles are exposed to adverse conditions, as seen in resistant plants, the percentage of males increase...

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Section: Discussionmentioning

confidence: 90%

A parasitic nematode releases cytokinin that controls cell division and orchestrates feeding site formation in host plants

Siddique

Radakovic

Torre

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

125

118

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“…The ancient pathways for auxin (Bennett et al 2014a(Bennett et al , 2014bFinet and Jaillais 2012;Paponov et al 2009), cytokinin (Lindner et al 2014;Pils and Heyl 2009;von Schwartzenberg et al 2007), and ethylene (Yasumura et al 2012) were investigated with respect to their corresponding transporters, biosynthesis, and signaling pathways. Further, moss is lacking essential characteristics of the classical gibberellin signaling pathway, although it responds to external gibberellin treatment (Vandenbussche et al 2007).…”

Section: Several Regulatory Pathways Evolved In the Common Ancestor Omentioning

confidence: 99%

Can mosses serve as model organisms for forest research?

Müller

Gütle

Jacquot

et al. 2016

Annals of Forest Science

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& Key message Based on their impact on many ecosystems, we review the relevance of mosses in research regarding stress tolerance, metabolism, and cell biology. We introduce the potential use of mosses as complementary model systems in molecular forest research, with an emphasis on the most developed model moss Physcomitrella patens. & Context and aims Mosses are important components of several ecosystems. The moss P. patens is a well-established nonvascular model plant with a high amenability to molecular biology techniques and was designated as a JGI plant flagship genome. In this review, we will provide an introduction to moss research and highlight the characteristics of P. patens and other mosses as a potential complementary model system for forest research. & Methods Starting with an introduction into general moss biology, we summarize the knowledge about moss physiology and differences to seed plants. We provide an overview of the current research areas utilizing mosses, pinpointing potential links to tree biology. To complement literature review, we discuss moss advantages and available resources regarding molecular biology techniques. & Results and conclusion During the last decade, many fundamental processes and cell mechanisms have been studied in mosses and seed plants, increasing our knowledge of plant evolution. Additionally, moss-specific mechanisms of stress tolerance are under investigation to understand their resilience in ecosystems. Thus, using the advantages of model mosses such as P. patens is of high interest for various research approaches, including stress tolerance, organelle biology, cell polarity, and secondary metabolism.

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“…The activity of tRNA‐IPT and an associated tRNA degradation process represents a conserved mechanism for CK production and accounts for the major portion of c Z in A. thaliana and P. patens (Miyawaki et al ., ; Lindner et al ., ). Consistently, homologous proteins have been identified in all living organisms, except Archaea (Spíchal, ).…”

Section: Discussionmentioning

confidence: 97%

“…This modification stabilizes codon-anticodon binding and thus enables precise protein biosynthesis (Konevega et al, 2006). The degradation of these modified tRNAs accounts for the major pool of cZ-type CKs in Arabidopsis thaliana and the moss Physcomitrella patens (Miyawaki et al, 2006;Lindner et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Functional characterization of the first filamentous fungal tRNA‐isopentenyltransferase and its role in the virulence of Claviceps purpurea

Hinsch¹,

Galuszka²,

Tudzynski³

2016

New Phytologist

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In plants, cytokinins (CKs) are synthesized de novo or by the degradation of modified tRNAs. Recently, the first fungal de novo pathway was identified within the plant pathogen Claviceps purpurea. As the deletion of the de novo pathway did not lead to a complete loss of CKs, this work focuses on the tRNA-modifying protein tRNA-isopentenyltransferase (CptRNA-IPT). The contribution of this enzyme to the CK pool of Claviceps and the role of CKs in the host-pathogen interaction are emphasized. The effects of the deletion of cptRNA-ipt and the double deletion of cptRNA-ipt and the key gene of de novo biosynthesis cpipt-log on growth, CK biosynthesis and virulence were analyzed. In addition, the sites of action of CptRNA-IPT were visualized using reporter gene fusions. In addition to CK-independent functions, CptRNA-IPT was essential for the biosynthesis of cis-zeatin (cZ) and contributed to the formation of isopentenyladenine (iP) and trans-zeatin (tZ). Although ΔcptRNA-ipt was reduced in virulence, the 'CK-free' double deletion mutant was nearly apathogenic. The results prove a redundancy of the CK biosynthesis pathway in C. purpurea for iP and tZ formation. Moreover, we show, for the first time, that CKs are required for the successful establishment of a host-fungus interaction.

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Isopentenyltransferase-1 (IPT1) knockout in Physcomitrella together with phylogenetic analyses of IPTs provide insights into evolution of plant cytokinin biosynthesis

Abstract: SummaryIs there more than one pathway for cytokinin biosynthesis in Physcomitrella? Despite the apparent absence of adenylate-isopentenyltransferases, characterization of ipt1 knockout mutants points towards a second, tRNA-independent cytokinin biosynthesis pathway.

Cited by 55 publications

References 71 publications

A parasitic nematode releases cytokinin that controls cell division and orchestrates feeding site formation in host plants

A parasitic nematode releases cytokinin that controls cell division and orchestrates feeding site formation in host plants

Can mosses serve as model organisms for forest research?

Functional characterization of the first filamentous fungal tRNA‐isopentenyltransferase and its role in the virulence of Claviceps purpurea

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