SMAX1-LIKE/D53 Family Members Enable Distinct MAX2-Dependent Responses to Strigolactones and Karrikins in Arabidopsis

Soundappan, Ishwarya; Bennett, Tom; Morffy, Nicholas; Liang, Yueyang; Stanga, John P.; Abbas, Amena; Leyser, Ottoline; Nelson, David C.

doi:10.1105/tpc.15.00562

Cited by 356 publications

(564 citation statements)

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“…Thus, as is the case in many other hormonal signaling pathways in plants, the regulated degradation of target proteins by the 26S proteasome appears to be a key feature of SL signaling. The principle proteolytic targets of SL signaling appear to be a clade of proteins in the SMAX1-LIKE (SMXL) family, typified by SMXL7 in Arabidopsis thaliana and D53 in rice (Oryza sativa) (Jiang et al, 2013;Zhou et al, 2013;Soundappan et al, 2015;Wang et al, 2015). SMXL proteins are weakly homologous to HEAT SHOCK PROTEIN101 ClpB chaperonins and are named for the founding member, SUPPRESSOR OF MAX2 1 (SMAX1) (Stanga et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

“…One of the best-characterized of these interactions is between the EAR motif in Aux/IAA proteins (repressors of auxin signaling) and the TOPLESS RELATED (TPR) family of chromatin remodeling factors (Szemenyei et al, 2008). The EAR motif in SMXL7 permits relatively weak interaction with TPR proteins, particularly TPR2 (Soundappan et al, 2015;Wang et al, 2015). On this basis, it has been suggested that SMXL proteins act as regulators of transcription (Smith and Li, 2014), but the functional relevance of this interaction, and indeed the EAR motif in general, has not been established.…”

Section: Introductionmentioning

confidence: 99%

“…SMAX1 is also a probable target of SCF MAX2 , although in this case in response to signaling mediated by the KAI2 receptor protein, itself a close relative of D14, for which the endogenous ligand is currently unknown Stanga et al, 2013;Soundappan et al, 2015). In Arabidopsis, SMXL7 is rapidly degraded in response to treatment with rac-GR24 in a D14-and MAX2-dependent manner (Soundappan et al, 2015;Wang et al, 2015). Furthermore, loss of SMXL7 function, in combination with that of its close relatives SMXL6 and SMXL8, is sufficient to suppress completely the SL-related shoot and root phenotypes of max2, suggesting that these proteins are the primary and probably only direct targets of MAX2-mediated SL signaling (Soundappan et al, 2015;Wang et al, 2015).…”

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confidence: 99%

“…Furthermore, loss of SMXL7 function, in combination with that of its close relatives SMXL6 and SMXL8, is sufficient to suppress completely the SL-related shoot and root phenotypes of max2, suggesting that these proteins are the primary and probably only direct targets of MAX2-mediated SL signaling (Soundappan et al, 2015;Wang et al, 2015). In line with both models of the regulation of shoot branching, the smxl6 smxl7 smxl8 max2 quadruple mutant has both strongly upregulated BRC1 expression and strongly downregulated PIN1 levels relative to max2 (Soundappan et al, 2015).SMXL proteins contain a well-conserved ETHYLENE-RESPONSE FACTOR Amphiphilic Repression (EAR) motif (Ohta et al, 2001), which has been widely viewed as an important contributor to SMXL function (Jiang et al, 2013;Zhou et al, 2013;Smith and Li, 2014;Soundappan et al, 2015;Wang et al, 2015), although this is based only on circumstantial evidence. EAR motifs allow proteins to interact with partners containing corresponding C-Terminal to Lissencephaly Homology (CTLH) domains (Szemenyei et al, 2008).…”

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confidence: 99%

“…Second, we created a protein deletion that removed the entire second NTPase domain (SMXL7 NTP2 ). Third, we modified the EAR motif (Leu-Asp-Leu-Asn-Leu-Pro) in SMXL7, either by deleting it (SMXL7 DEAR ) or by replacing the conserved 1584 The Plant Cell leucine residues with alanines (Ala-Asp-Ala-Asn-Ala-Pro; SMXL7 alaEAR ), which has previously been shown to abolish its interaction with TPR2 in yeast two-hybrid assays (Soundappan et al, 2015). We also created two double deletions of both the P-loop and the EAR motif (SMXL7 DP-loop,DEAR and SMXL7 d53,alaEAR ).…”

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SMAX1-LIKE7 signals from the nucleus to regulate shoot development in Arabidopsis via partially EAR motif-independent mechanisms

et al. 2016

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Strigolactones (SLs) are hormonal signals that regulate multiple aspects of shoot architecture, including shoot branching. Like many plant hormonal signaling systems, SLs act by promoting ubiquitination of target proteins and their subsequent proteasome-mediated degradation. Recently, SMXL6, SMXL7, and SMXL8, members of the SMAX1-LIKE (SMXL) family of chaperonin-like proteins, have been identified as proteolytic targets of SL signaling in Arabidopsis thaliana. However, the mechanisms by which these proteins regulate downstream events remain largely unclear. Here, we show that SMXL7 functions in the nucleus, as does the SL receptor, DWARF14 (D14). We show that nucleus-localized D14 can physically interact with both SMXL7 and the MAX2 F-box protein in a SL-dependent manner and that disruption of specific conserved domains in SMXL7 affects its localization, SL-induced degradation, and activity. By expressing and overexpressing these SMXL7 protein variants, we show that shoot tissues are broadly sensitive to SMXL7 activity, but degradation normally buffers the effect of increasing SMXL7 expression. SMXL7 contains a well-conserved EAR (ETHYLENE-RESPONSE FACTOR Amphiphilic Repression) motif, which contributes to, but is not essential for, SMXL7 functionality. Intriguingly, different developmental processes show differential sensitivity to the loss of the EAR motif, raising the possibility that there may be several distinct mechanisms at play downstream of SMXL7. INTRODUCTIONShoot system architectural characteristics strongly influence the productivity of many crop species, and architectural traits have been selected in both historical and contemporary breeding schemes. Understanding the mechanisms that regulate shoot architecture, and its environmental responsiveness, is therefore an important goal for plant research. It is well established that long-distance hormonal signals, including auxin, cytokinin, and strigolactone (SL), are key regulators of shoot architecture and allow communication both within the shoot system and between the shoot and root . For instance, cytokinin produced in the root system in response to the availability of nitrate ions is systemically transported to the shoot, where it promotes branching (Kiba et al., 2011; Müller et al., 2015). Similarly, root-derived SL plays a key role in negatively regulating branching in response to low phosphate availability in the rhizosphere (Kohlen et al., 2011). However, our understanding of the molecular mechanisms that act downstream of these hormones to alter developmental processes in the shoot is currently limited. This is particularly true of SLs. Analysis of the phenotypes of SL biosynthesis and signaling mutants has revealed roles for SLs in the regulation of shoot branching, branching angle, plant height, stem thickness, and leaf blade elongation . The role of SLs in regulating shoot branching has been intensively studied, resulting in two contrasting, nonexclusive models for their mode of action. In the first, SLs are proposed to act locally in axill...

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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confidence: 99%

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confidence: 99%

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SMAX1-LIKE7 signals from the nucleus to regulate shoot development in Arabidopsis via partially EAR motif-independent mechanisms

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Karrikins: Germination Stimulants Produced by Wildfires

Smith¹

2019

Encyclopedia of Life Sciences

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Karrikins are simple organic chemicals produced by wildfires that stimulate germination of dormant seeds in the soil. They are present in the smoke and char produced by the fire and are washed into the soil by the following rains. Many plant species have evolved such that their seeds remain dormant in the soil until they encounter karrikins, whereupon they can germinate. This strategy has the advantage that emerging seedlings will have plenty of light and a supply of nutrients released by the fire. Such plants are termed ‘fire ephemerals’ because they appear after fires, then flower, produce seed and die. It is believed that karrikins mimic an unidentified endogenous germination hormone. Karrikins are also similar to endogenous hormones called strigolactones that control plant development. Karrikin perception by seeds apparently requires a protein closely related to the strigolactone receptor. Karrikins or smoke can be used to stimulate germination in horticulture and landscape revegetation. Key Concepts Wildfires stimulate seeds in the soil to germinate which contributes to rapid revegetation. Seeds from many plant species are adapted to respond to chemicals produced by fire. The most active germination stimulant produced by wildfires is a butenolide named ‘karrikin’. Karrikins can influence germination and also seedling development. The receptor protein and molecular components of the response pathway have been identified. Karrikins mimic an ancient endogenous plant hormone that has not yet been identified. Karrikins stimulate germination of agricultural weeds and so might be useful for their control. Karrikins provide tools and knowledge to help us manage our natural landscapes. Karrikins might be useful in seed conservation work and in seed banks. The karrikin signalling system might be applied in crop breeding for environmental resilience.

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Genetic dissection of cell wall defects and the strigolactone pathway in Arabidopsis

Ramírez

Pauly

2019

Plant Direct

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Defects in the biosynthesis and/or deposition of secondary plant cell wall polymers result in the collapse of xylem vessels causing a dwarfed plant stature and an altered plant architecture termed irregular xylem ( irx ) syndrome. For example, reduced xylan O ‐acetylation causes strong developmental defects and increased freezing tolerance. Recently, we demonstrated that the irx syndrome in the trichome birefringence‐like 29/eskimo1 ( tbl29/esk1 ) mutant is dependent on MORE AXILLARY GROWTH 4 ( MAX 4), a key enzyme in the biosynthesis of the phytohormone strigolactone ( SL ). In this report, we show that other xylan‐ and cellulose‐deficient secondary wall mutants exhibit increased freezing tolerance correlated with the irx syndrome. In addition, these phenotypes are also dependent on MAX 4, suggesting a more general interaction between secondary wall defects and SL biosynthesis. In contrast, MAX 4 does not play a role in developmental defects triggered by primary wall deficiencies, suggesting that the interaction is restricted to vascular tissue. Through a reverse genetics approach, the requirement of different components of the SL pathway impacting the irx syndrome in tbl29 was evaluated. Our results show that the tbl29 ‐associated irx phenotypes are dependent on the MAX 3 and MAX 4 enzymes, involved in the early steps of SL biosynthesis. In contrast, this signaling is independent on downstream enzymes in the biosynthesis and perception of SL such as MAX 1 and MAX 2.

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SMAX1-LIKE/D53 Family Members Enable Distinct MAX2-Dependent Responses to Strigolactones and Karrikins in Arabidopsis

Cited by 356 publications

References 79 publications

SMAX1-LIKE7 signals from the nucleus to regulate shoot development in Arabidopsis via partially EAR motif-independent mechanisms

SMAX1-LIKE7 signals from the nucleus to regulate shoot development in Arabidopsis via partially EAR motif-independent mechanisms

Karrikins: Germination Stimulants Produced by Wildfires

Genetic dissection of cell wall defects and the strigolactone pathway in Arabidopsis

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