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WIND transcription factors orchestrate wound-induced callus formation, vascular reconnection and defense response in Arabidopsis

Iwase, Akira Kondo, Yuki Laohavisit, Anuphon Takebayashi, Arika Ikeuchi, Momoko Matsuoka, Keita Asahina, Masashi Mitsuda, Nobutaka Shirasu, Ken Fukuda, Hiroo Sugimoto, Keiko 神戸大学

2021.08.10

概要

Wounding is a serious threat to the plant survival and it triggers multiple physiological responses to quickly heal and protect dam- aged tissues from pathogen invasion (Reymond et al., 2000; Cheong et al., 2002). In plants, formation of a pluripotent cell mass, called callus, at wound sites is often a key step to regenerate new organs and develop physical and chemical barriers against pathogens (Birnbaum & Alvarado, 2008; Asahina et al., 2011; Ikeuchi et al., 2013, 2016; Melnyk, 2017). Importantly, wound- ing and callus formation is often accompanied by vascular refor- mation presumably to establish the route for water and nutrient transport in developing cell mass (Fukuda, 1997; Mazur et al., 2016). Accordingly, earlier studies reported ectopic tracheary ele- ment formation in the genetic tumor of Nicotiana tabacum callus (White, 1939) and crown galls (Van Lith-Vroom et al., 1960). It is also known that grafted plants initially form callus at wound sites, followed by vascular bundle reformation within callus (Mel- nyk et al., 2015; Melnyk, 2017). Surface regeneration of debarked tree trunk is another well-characterized regeneration phenomenon after wounding where xylem and phloem reforma- tion occur after callus formation (Stobbe et al., 2002). Although we have made considerable progress in our understanding of how plants perceive wounding signals (Toyota et al., 2018; Ikeuchi et al., 2019, 2020; Marhava et al., 2019), our knowledge on how plants initiate such a diverse array of wound-induced responses is still very limited (Bloch, 1941; Walker-Simmons et al., 1984; Savatin et al., 2014).

　Given that these wound-induced events require dynamic changes in gene expression, it is likely that plants possess some transcriptional mechanisms to coordinate their progression. Recent studies have indeed identified several wound-inducible transcription factors that have critical roles in regeneration (Ikeuchi et al., 2013, 2016, 2019; Xu & Huang, 2014). We pre- viously reported that an APETALA2/ETHYLANE RESPONSE FACTOR (AP2/ERF) transcription factor WOUND INDUCED DEDIFFERENTIATION 1 (WIND1) and its close homologs, WIND2, WIND3 and WIND4, promote wound- induced callus formation through activating the cytokinin response (Iwase et al., 2011a,b, 2013, 2015). WIND1 also pro- motes shoot regeneration via direct activation of another AP2/ ERF transcription factor ENHANCER OF SHOOT REGENERATION 1 (ESR1) (Iwase et al., 2017, 2018). WIND induction, in addition, leads to somatic embryogenesis on phytohormone-free medium (Ikeuchi et al., 2013), implying that WIND1 can drive multiple developmental pathways to promote regeneration. At the cellular level, WIND1 promotes the acquisi- tion of regenerative competence since ectopic overexpression of WIND1 can bypass wounding and early incubation steps on auxin-rich callus inducing medium (CIM), which are the prereq- uisite for shoot regeneration on cytokinin-rich shoot inducing medium (SIM) (Valvekens et al., 1988; Iwase et al., 2015). Sev- eral other AP2/ERF family transcription factors are also impli- cated in the control of regeneration since PLETHORA3 (PLT3), PLT5 and PLT7, are critical for wound-induced callus formation and pluripotency acquisition under CIM/SIM condition (Kareem et al., 2015; Ikeuchi et al., 2017, 2020). Another wound-inducible AP2/ERF protein ETHYLENE RESPONSE FACTOR 115 (ERF115), acting upstream of WIND1, is required for reformation of root stem cells and regeneration of root meristems after injury (Heyman et al., 2013, 2016; Marhava et al., 2019; Zhou et al., 2019). ERF113/RELATED TO AP2 6 LIKE (RAP2.6L), which is a close homolog of ERF115, is reported as a key regulator of tissue reconnection process (Asahina et al., 2011) as well as for shoot regeneration under CIM/SIM condition (Che et al., 2006).

　Several important transcriptional regulators of plant vascular development have also been identified (Kondo, 2018) and for instance, VASCULAR-RELATED NAC-DOMAIN6 (VND6) and VND7 transcription factors function as master regulators for the formation of vascular vessels (Kubo et al., 2005). Overexpres- sion of VND6 or VND7 provokes ectopic tracheary element for- mation in diverse cell types (Kubo et al., 2005). LATERAL ORGAN BOUNDARIES DOMAIN 30 (LBD30), a putative positive feedback regulator for VND6 and VND7, also shows similar ectopic tracheary formation when overexpressed in Ara- bidopsis thaliana (Arabidopsis) (Soyano et al., 2008). Other Ara- bidopsis NAC domain transcription factors ANAC071 and ANAC091 are required in tissue reconnection and conversion of mesophyll cell fate to cambial cells (Asahina et al., 2011; Mat- suoka et al., 2021). Recent studies using the in vivo and in vitro culturing system have started to unveil further transcriptional reg- ulatory networks driving the vascular development (Kondo et al., 2016; Miyashima et al., 2019). When Arabidopsis leaf tissues are incubated under the Vascular Cell Induction Culture System Using Arabidopsis Leaves (VISUAL), leaf mesophyll cells reprogram into vascular cells and start to express cambium cell marker genes such as TDIF RECEPTOR (TDR) and Arabidopsis thaliana HOMEOBOX GENE8 (AtHB8) (Kondo et al., 2016). This is followed by the upregulation of xylem marker genes, such as IRREGULAR XYLEM3 (IRX3), and phloem marker genes such as SIEVE-ELEMENT-OCCLUSION-RELATED1 (SEOR1). Despite these progresses, whether these key regulators contribute to xylem formation after wounding and if so, how wounding activates these regulators remain unknown.

　Hierarchal transcriptional networks acting from pathogen per- ception to the immune responses (Cui et al., 2015) are well char- acterized and many WRKY transcription factors are known to play major roles in defense signaling (Eulgem & Somssich, 2007). WRKY18 and WRKY53, for instance, positively regulate defense responses and these regulators induce genes for key enzymes in biosynthesis of phytoalexins, the antimicrobial sec- ondary metabolites (Wang et al., 2006; Murray et al., 2007). Camalexin, a well-known phytoalexin in Arabidopsis, is synthe- sized de novo after various biotic and abiotic stress including pathogen infection (Ahuja et al., 2012). P450 monooxygenases, Cytochrome P450 71B15 (CYP71B15/PAD3) and CYP71A13, are involved in camalexin biosynthesis and they are induced after pathogen infection in a WRKY33-dependent manner (Qiu et al., 2008). A single knock-out mutation of these P450 monooxyge- nases enhances disease susceptibility against bacterial pathogen infection (Rajniak et al., 2015).

　Lysine-derived pipecolic acid is a critical regulator for an estab-lishment of systemic acquired resistance in Arabidopsis upon pathogen infection, and is synthesized via AGD2-LIKE DEFENSE REPONSE PROTEIN 1 (ALD1) (Hartmann et al., 2018). ALD1 also shows WRKY33-dependent expression man- ner, and importantly, plants defective in this gene show higher susceptibility to pathogens (Song et al., 2004; N´avarov´a et al., 2012; Wang et al., 2018), indicating that the control of WRKY- mediated phytoalexin and signal molecule production are crucial for the defense response.

　Interestingly, ERF108/RELATED TO AP2 6 (RAP2.6), a close homolog of ERF115 and RAP2.6L in the subfamily X of AP2/ERF transcription factors, may function in the defense response since its expression is strongly induced after challenged with a virulent Pseudomonas syringae pv. tomato DC3000 (Pst DC3000). ERF108/RAP2.6 also promotes resistance against cyst nematode infection though the enhancement of callose deposi- tion in Arabidopsis (He et al., 2004; Ali et al., 2013). These find- ings highlight the multifaceted roles of AP2/ERF transcription factors in tissue repair and defense responses (Heyman et al., 2018) but how their stress-induced expression is regulated remains to be elucidated.

　Several recent transcriptome studies revealed that the wound- induced transcriptional changes highly overlap with those elicited by various biotic and abiotic stresses (Cheong et al., 2002; Ikeuchi et al., 2017; Melnyk et al., 2018), suggesting the existence of com- mon regulators that function in multiple stress responses. Given that callus produced by constitutive WIND1 expression shows increased expression of some vascular genes and defense response genes (Iwase et al., 2011a), it is plausible that WIND1 and its homologs play diverse roles in response to wounding and other forms of stress. In this study we conducted the time-course tran- scriptome analyses after WIND1 induction to explore how WIND1 functions in stress response. Our data show that WIND1 transcriptionally activates over 2000 genes implicated in cellular reprogramming, vascular formation and defense response. Further functional analyses confirmed that WIND transcription factors have important roles during wound-induced cellular reprogram- ming, vascular regeneration and defense response. Our results, therefore, provide important molecular insights into how plants coordinately control regeneration and innate immunity through WIND-mediated transcriptional mechanisms.

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