Selective Autophagy of BES1 Mediated by DSK2 Balances Plant Growth and Survival

Nolan, Trevor M.; Brennan, Benjamin; Yang, Mofeng; Chen, Jiani; Zhang, Mingcai; Li, Zhaohu; Wang, Xuelu; Bassham, Diane C.; Walley, Justin W.; Yin, Yanhai

doi:10.1016/j.devcel.2017.03.013

Cited by 276 publications

(336 citation statements)

References 85 publications

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“…Thus, growth and stress responses are generally antagonistic processes, and plants must balance the two during their life cycle (Heidel et al, 2004;Achard et al, 2006;Claeys & Inz e, 2013). Much is known about the regulatory mechanisms involved in plant growth and stress responses, but little is known about the mechanisms that coordinate these processes (Skirycz et al, 2011;Nolan et al, 2017). To maintain an appropriate balance between growth and stress responses under normal or stressful conditions, plants must adjust their growth and stress response programs.…”

Section: Researchmentioning

confidence: 99%

SKIP regulates environmental fitness and floral transition by forming two distinct complexes in Arabidopsis

Yang

Shang

et al. 2019

New Phytologist

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Summary Ski‐interacting protein (SKIP) is a bifunctional regulator of gene expression that works as a splicing factor as part of the spliceosome and as a transcriptional activator by interacting with EARLY FLOWERING 7 (ELF7). MOS4‐Associated Complex 3A (MAC3A) and MAC3B interact physically and genetically with SKIP, mediate the alternative splicing of c. 50% of the expressed genes in the Arabidopsis genome, and are required for the splicing of a similar set of genes to that of SKIP. SKIP interacts physically and genetically with splicing factors and Polymerase‐Associated Factor 1 complex (Paf1c) components. However, these splicing factors do not interact either physically or genetically with Paf1c components. The SKIP‐spliceosome complex mediates circadian clock function and abiotic stress responses by controlling the alternative splicing of pre‐mRNAs encoded by clock‐ and stress tolerance‐related genes. The SKIP‐Paf1c complex regulates the floral transition by activating FLOWERING LOCUS C (FLC) transcription. Our data reveal that SKIP regulates floral transition and environmental fitness via its incorporation into two distinct complexes that regulate gene expression transcriptionally and post‐transcriptionally, respectively. It will be interesting to discover in future studies whether SKIP is required for integration of environmental fitness and growth by control of the incorporation of SKIP into spliceosome or Paf1c in plants.

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Section: Researchmentioning

confidence: 99%

SKIP regulates environmental fitness and floral transition by forming two distinct complexes in Arabidopsis

Yang

Shang

et al. 2019

New Phytologist

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“…DSK2 (UBL and DSK2b proteins reached 99% homology at amino acid sequence level in maize) also plays an important role in plant growth and survival in A. thaliana . The drought resistance of a DSK2 RNAi line decreased substantially and this stress response phenotype was similar with accumulation of UBL in maize increased its resistance against pathogen (Nolan et al ). Intriguingly, Hyd1 promoted the accumulation of UBL and caused cell death in maize and tomato (Figure S8).…”

Section: Discussionmentioning

confidence: 91%

Elicitor hydrophobin Hyd1 interacts with Ubiquilin1‐like to induce maize systemic resistance

Dou

Wang

et al. 2019

JIPB

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Trichoderma harzianum is a plant‐beneficial fungus that secretes small cysteine‐rich proteins that induce plant defense responses; however, the molecular mechanism involved in this induction is largely unknown. Here, we report that the class II hydrophobin ThHyd1 acts as an elicitor of induced systemic resistance (ISR) in plants. Immunogold labeling and immunofluorescence revealed ThHyd1 localized on maize (Zea mays) root cell plasma membranes. To identify host plant protein interactors of Hyd1, we screened a maize B73 root cDNA library. ThHyd1 interacted directly with ubiquilin 1‐like (UBL). Furthermore, the N‐terminal fragment of UBL was primarily responsible for binding with Hyd1 and the eight‐cysteine amino acid of Hyd1 participated in the protein‐protein interactions. Hyd1 from T. harzianum (Thhyd1) and ubl from maize were co‐expressed in Arabidopsis thaliana, they synergistically promoted plant resistance against Botrytis cinerea. RNA‐sequencing analysis of global gene expression in maize leaves 24 h after spraying with Curvularia lunata spore suspension showed that Thhyd1‐induced systemic resistance was primarily associated with brassinosteroid signaling, likely mediated through BAK1. Jasmonate/ethylene (JA/ET) signaling was also involved to some extent in this response. Our results suggest that the Hyd1‐UBL axis might play a key role in inducing systemic resistance as a result of Trichoderma‐plant interactions.

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“…Mutants that disrupt some ATG genes or receptors of autophagy are hypersensitive to or have reduced survival in nitrogen or carbon starvation assays 17, 22, 61 . Thus, we assayed the response of the single, double and triple mutants of EXO70D s to carbon starvation.…”

Section: Resultsmentioning

confidence: 99%

“…For example, in response to sulfur stress, Joka2, a tobacco member of the family of selective autophagy cargo receptors, triggers the autophagic degradation of the sulfur responsive protein, UPC9, by interacting with both UPC9 and ATG8f 20 . Selective autophagy also regulates rubisco degradation during leaf senescence 21 , brassinosteroid responses via targeting of BRI1-EMS SUPPRESSOR 1 (BES) by DOMINANT SUPPRESSOR OF KAR2 (DSK2) 22 , and ATG8-INTERACTING PROTEIN 1 (ATI1)-mediated turnover of plastid proteins 23 .…”

Section: Introductionmentioning

confidence: 99%

EXO70D isoforms mediate selective autophagic degradation of Type-A ARR proteins to regulate cytokinin sensitivity

Acheampong

Shanks

Chang

et al. 2020

Preprint

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19The phytohormone cytokinin influences many aspects of plant growth and development, several of 20 which also involve the cellular process of autophagy, including leaf senescence, nutrient re-21 mobilization, and developmental transitions. The Arabidopsis type-A Response Regulators (type-A 22 ARR) are negative regulators of cytokinin signaling that are transcriptionally induced in response to 23 cytokinin. Here, we describe a mechanistic link between cytokinin signaling and autophagy, 24 demonstrating that plants modulate cytokinin sensitivity through autophagic regulation of type-A 25 ARR proteins. Type-A ARR proteins were degraded by autophagy in an AUTOPHAGY-RELATED 26 (ATG)5-dependent manner. EXO70D family members interacted with Type-A ARR proteins, likely 27 in a phosphorylation-dependent manner, and recruited them to autophagosomes via interaction with 28 the core autophagy protein, ATG8. Consistently, loss-of-function exo70D1,2,3 mutants 29 compromised targeting of type-A ARRs to autophagic vesicles, have elevated levels of type-A ARR 30 proteins, and are hyposensitive to cytokinin. Disruption of both type-A ARRs and EXO70D1,2,3 31 compromised survival in carbon-deficient conditions, suggesting interaction between autophagy and 32 cytokinin responsiveness in response to stress. These results indicate that the EXO70D proteins act 33 as selective autophagy receptors to target type-A ARR cargos for autophagic degradation, 34 demonstrating that cytokinin signaling can be modulated by selective autophagy. 35 36 37Autophagy is a major catabolic pathway that maintains cellular homeostasis in response to 38 intrinsic developmental changes and environmental cues. It mediates the degradation of protein 39 complexes, misfolded and aggregated proteins, and damaged organelles by targeting proteins to 40 proteases localized in the vacuole or lysosome, with a subsequent retro-transport of cellular building 41 blocks back into the cytosol 1-3 . There are three main types of autophagy: macro-, micro-and 42 chaperon-mediated autophagy 1,4,5 . Macro-autophagy (hereafter referred to simply as autophagy) is 43 mediated by conserved AUTOPHAGY-RELATED GENEs (ATGs) that coordinate the de novo 44 biogenesis of the autophagy organelle, the autophagosome 6-8 . Autophagosomes are double 45 membrane vesicles that sequester various cargoes and ultimately deliver them to the lytic vacuole, 46 resulting in their degradation and subsequent recycling. Although basal autophagy occurs in cells 47 under steady-state conditions 9,10 , it is enhanced in response to biotic and abiotic stresses 11-13 and can 48 result in selective or bulk (non-selective) degradation of proteins 4 . Typically, bulk autophagy 49 randomly degrades cytosolic content, while selective autophagy requires unique receptors to target 50 specific cargos for degradation 14,15 . These receptors contain the unique ATG8-INTERACTING 51 MOTIFs (AIM) or LIR-INTERACTING MOTIFs that allow them to interact with the ATG proteins 52 on the autophagosomal membrane 16 . They also...

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Selective Autophagy of BES1 Mediated by DSK2 Balances Plant Growth and Survival

Cited by 276 publications

References 85 publications

SKIP regulates environmental fitness and floral transition by forming two distinct complexes in Arabidopsis

SKIP regulates environmental fitness and floral transition by forming two distinct complexes in Arabidopsis

Elicitor hydrophobin Hyd1 interacts with Ubiquilin1‐like to induce maize systemic resistance

EXO70D isoforms mediate selective autophagic degradation of Type-A ARR proteins to regulate cytokinin sensitivity

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