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Spotlight
Are karrikins involved in plant abiotic stress responses? Weiqiang Li and Lam-Son Phan Tran Signaling Pathway Research Unit, RIKEN Center for Sustainable Resource Science, 1-7-22, Suehiro-cho, Tsurumi, Yokohama 230-0045, Japan
Recent reports have shown that strigolactones play a positive role in plant responses to drought and salt stress through MAX2 (More Axillary Growth 2). Increasing evidence suggests that MAX2 is also involved in karrikin signaling, raising the question whether karrikins play any role in plant adaptation to abiotic stresses.
MAX2: a mediator between strigolactone and karrikin signaling Strigolactones are new plant hormones that are known as root-derived signals for parasitic plant seed germination and arbuscular mycorrhizal fungi hyphal elongation [1]. In addition, strigolactones are involved in regulation of many biological processes in host plants, from growth and development to responses to environmental stresses [1]. In Arabidopsis (Arabidopsis thaliana), at least four genes have been discovered to be involved in strigolactone biosynthesis, namely AtD27 (Arabidopsis thaliana DWARF27), MAX3 (More Axillary Growth 3), MAX4 and MAX1 [1]. AtD27 was demonstrated to catalyze the reversible isomerization of all-trans-b-carotene at C-9-position to yield 9-cis-b-carotene. MAX3 preferentially cleaves 9-cis-b-carotene to produce 9-cis-b-apo-100 -carotenal that is then cleaved by MAX4 to form carlactone (Figure 1A). Carlactone is a compound that carries the methylbutenolide part of strigolactones and exhibits strigolactone-like biological activities [1]. In Arabidopsis, carlactone was shown to be converted to carlactonoic acid by MAX1 (Figure 1A) [2]. However, in rice (Oryza sativa) carlactone was reported to be catalyzed to strigolactones (orobanchol) by at least two MAX1 homologs (Os01g0700900 and Os01g0701400) through two steps (Figure 1A) [3]. Strigolactones are perceived and transduced through multi-genic signaling, with two positive regulators and one negative regulator as central and direct components. One positive regulator was named D14 (DWARF14) in rice and AtD14 in Arabidopsis [1,4]. AtD14 is an a/b hydrolase fold protein that was suggested to be a putative strigolactone receptor (Figure 1B) [1,4]. Another positive regulator is called MAX2 in Arabidopsis and D3 (DWARF3) in rice which is an F-box protein capable of binding to AtD14 in a strigolactone-dependent manner [1,4]. Intensive studies have indicated that MAX2 is a key protein, playing important Corresponding author: Tran, L.-S. (
[email protected]). Keywords: strigolactones; karrikins; abiotic stress responses. 1360-1385/ ß 2015 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tplants.2015.07.006
roles in both karrikin and strigolactone signaling pathways in Arabidopsis [4]. As for the negative regulator or suppressor of the strigolactone signaling, a great step forward came with the analysis of d53 (dwarf53) rice mutant, which showed that degradation of D53 inhibited shoot branching through interaction with D14 and D3/MAX2 in a strigolactone-dependent manner (Figure 1B) [5]. D53 is somewhat similar to the HSP101 (HEAT SHOCK PROTEIN 101) of the Clp ATPase family of nine members in rice [5]. Karrikins have been purified from burnt plant materials and shown to promote seed germination [4]. In addition to promoting seed germination, karrikins are also involved in inhibition of hypocotyl elongation, promotion of cotyledon expansion and greening, as well as in increase of seedling vigor and alleviation of seed germination under stressful environments [4,6]. The discovery that karrikins are active in plants has suggested that karrikins could be mimicking an endogenous signaling molecule [4]. In Arabidopsis, two genes, MAX2 and KAI2 (Karrikin Insensitive 2), were found to be essential for the karrikin responses [4] (Figure 1C). KAI2 encodes an a/b hydrolase fold protein with similar structure to AtD14, and thus also called AtD14-like. The binding assay and phenotype analysis suggested that KAI2 might be a putative karrikin receptor [4]. KAI2 and AtD14 specifically mediate plant responses to karrikins and canonical, natural strigolactones, respectively [4]. Similar to what was found in strigolactone signaling, a protein, named SMAX1 (Suppressor of MAX2 1), was identified as a suppressor of karrikin signaling in Arabidopsis [7]. Unlike D53, SMAX1 was reported to play a role in seed germination and hypocotyl elongation through KAI2MAX2 signaling, but not in shoot branching that is controlled by AtD14-MAX2 signaling activated by canonical, natural strigolactones, suggesting that SMAX1 is a specific repressor of the karrikin signaling [7]. Indeed, there is no evidence either that would support a connection between SMAX1 and AtD14. Like D53 of rice, SMAX1 is also a member of the Clp ATPase family in Arabidopsis that has eight members, and the other members are named SMAX1-like2-8 (SMXL2-8) [7]. D53/SMXL family members might have distinct roles in plant development and some of them might be targeted for degradation by karrikin signaling and perhaps also strigolactone signaling [4]. Taken together, these findings indicate the existence of similar perception mechanisms and perhaps crosstalk between karrikin and strigolactone signaling pathways through the mediator MAX2. Plants possess similar mechanisms involving closely related receptors (KAI2 and AtD14) and suppressors (D53 and SMAX1), as well as a Trends in Plant Science xx (2015) 1–3
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O D10/ MAX4
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Seed germinaon, hypocotyl elongaon, leaf development, root development, and abioc stress TRENDS in Plant Science
Figure 1. Strigolactone biosynthesis, and strigolactone and karrikin perception modules. (A) Proposed model for strigolactone biosynthesis in Arabidopsis and rice. Carlactone is synthesized from all-trans-b-carotene by three enzymes, D27 (DWARF27)/AtD27, D17/MAX3 (More Axillary Growth 3) and D10/MAX4 in rice and Arabidopsis, respectively. Carlactone is converted to strigolactones (orobanchol) by MAX1 homologs (Os01g0700900 and Os01g0701400) in rice. In Arabidopsis, MAX1 catalyzes the conversion of carlactone to carlactonoic acid. Red- and green-colored characters indicate proteins of rice and Arabidopsis, respectively. (B) Strigolactones, after entering a cell, are bound by the a/b-hydrolase fold protein D14/AtD14 (AtD14 is an Arabidopsis ortholog of the rice D14), triggering a conformational change in D14/AtD14. Activated D14/AtD14 then interacts with the F-box protein D3/MAX2 (D3 is the rice ortholog of Arabidopsis MAX2) in the SCFD3/MAX2–E2 complex that tags class I Clp-ATPase D53/ SMXL [SMAX1 (Suppressor of MAX2 1)-like protein] (Arabidopsis ortholog of rice D53 is unknown, and it might be a SMXL) through polyubiquitination, resulting in degradation of D53. This subsequently leads to induction of strigolactone-responsive genes, resulting in repression of shoot branching, promotion of senescence and secondary thickening, alteration of root growth, and enhancement of stress tolerance. (C) In Arabidopsis, karrikins, after entering a cell, are bound by the a/b-hydrolase fold protein KAI2 (Karrikin Insensitive 2 or AtD14-like is an Arabidopsis ortholog of the rice D14-like), triggering a conformational change in KAI2. Activated KAI2 then interacts with the F-box protein MAX2 in the SCFMAX2–E2 complex that tags class I Clp-ATPase SMAX1 (D53-like rice ortholog of Arabidopsis SMAX1 is unknown) through polyubiquitination, resulting in degradation of SMAX1. This subsequently leads to induction of karrikin-responsive genes, resulting in inhibition of hypocotyl elongation, promotion of seed germination, alteration of leaf and root hair growth, and potentially enhancement of stress tolerance. Red color indicates that the karrikin-dependent molecular mechanisms regulating abiotic stress responses are still unknown. Abbreviations: E2, ubiquitin-conjugating enzyme; SCF, Skp–Cullin–F-box protein complex; U, ubiquitin.
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Spotlight common F-box protein MAX2 for perception of these two compounds (Figure 1B,C) [4]. Do karrikins play a role in plant responses to environmental stresses? Strigolactone was first shown to play a role in regulation of abiotic stresses, namely drought and salt stress, through a genetic study of strigolactone-deficient max3 and max4 mutants in Arabidopsis [8]. This finding was recently verified by a study using a strigolactone-deficient Lotus japonicus transgenic plant having Ljccd7 (Lotus japonicus carotenoid cleavage dioxygenase 7 encoding a MAX3 homolog) gene silenced [9]. To further support the involvement of strigolactone in controlling plant adaptation to abiotic stresses, several groups, including ours, also showed that the strigolactone signaling member MAX2 plays an important role in plant adaptation to drought and salt stress [8,10]. Given that MAX2 appears to be a crucial point of crosstalk between strigolactone and karrikin signaling pathways, these findings raise the interesting question whether karrikins play any role in plant adaptation to abiotic stresses. Several studies have reported that smokewater and butenolide could alleviate seed germination and seedling growth under high temperature, high salinity and low osmotic potential [6,11], suggesting that karrikins may play a role in plant responses to environmental stresses. However, how karrikins are involved in stress responses and by what mechanisms remains elusive. Transcriptome analysis of maize kernels treated with smoke-water showed transcriptome changes mimicking that of the stress hormone abscisic acid (ABA) [12]. Additionally, a comparative microarray analysis of Arabidopsis max2 and wild-type plants under dehydration also identified a number of dehydration- and/or ABA-inducible genes downregulated in max2 mutant [8]. These finding together suggest that karrikins might play a similar role to that of ABA in plant adaptations to abiotic stresses. This could be further verified by genetic studies of karrikin signalingrelated or specific mutants, such as kai2 mutant, under various stresses. Concluding remarks Significant progress has been made in the understanding of strigolactone biosynthesis and perception in the past few years [1–4]. However, studies on the role of strigolactones
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in plant adaptation to major environmental stresses, namely drought and salt stress, have just started [8– 10]. Identifying further members of strigolactone and karrikin signaling pathways and studying either common or specific members (e.g., AtD14, KAI2, D53, SMAX1, and SMXLs), will enable us to gain a better insight into molecular mechanisms underlying the roles of strigolactones and karrikins, as well as their role in plant adaptation to abiotic stresses. These efforts in turn will provide us a promising avenue for developing improved stress-tolerant crop plants. Acknowledgments We apologize to those colleagues who have contributed to this field but were not cited because of space limitations.
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