Autophagy and multivesicular body pathways cooperate to protect sulfur assimilation and chloroplast functions
Autophagy and multivesicular body pathways cooperate to protect sulfur assimilation and chloroplast functions
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自噬和多泡体途径协同保护硫同化和叶绿体功能
DOI：
10.1093/plphys/kiad133
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发表时间：
2023
期刊：
影响因子：
7.4
通讯作者：
Chen, Zhixiang
中科院分区：
文献类型：
--
作者：
Fu, Yunting;Fan, Baofang;Li, Xifeng;Bao, Hexigeduleng;Zhu, Cheng;Chen, Zhixiang
自噬和多泡小体(MVB)代表着两条密切相关的溶酶体/空泡降解途径。在拟南芥中，自噬是由胁迫诱导的，自噬缺陷会导致胁迫反应的强烈缺陷，但对生长的影响有限。Lyst相互作用蛋白5(LIP5)是胁迫诱导的MVB生物发生的关键调控因子，LIP5的突变也强烈地影响了胁迫反应，但对拟南芥的生长几乎没有影响。为了确定这两条途径在拟南芥中的功能相互作用，我们在LIP5和AUTOPHAGY相关蛋白(ATG)基因上都产生了突变。atg5/lip5和datg7/lip5双突变体在适应能力方面表现出很强的协同表型，其特征是生长受阻，衰老早，存活率降低，在正常生长条件下种子产量大大减少。转录组和代谢物分析表明，在可见表型出现之前，theg7/lip5双突变体的叶绿体硫酸盐同化作用在苗期早期被特异性下调。硫酸盐同化过程中的关键酶--腺苷5‘-磷酸硫酸盐还原酶1的过表达显著提高了theatg7/lip5双突变体的生长和适合度。比较多组体分析进一步表明，theg7/lip5双突变体在光合作用和初级碳代谢等其他叶绿体功能上受到严重损害。Atg/lip5双突变体的过早衰老和存活率降低与活性氧的积累和应激相关程序的过度激活有关。阻断植物抗病蛋白缺失4和水杨酸信号转导途径，可防止theatg7/lip5双突变体的早衰和死亡。因此，胁迫响应自噬和MVB途径在保护叶绿体的基本功能，包括正常生长条件下硫的同化，抑制依赖水杨酸的细胞过早死亡，促进植物生长和适应方面发挥着重要的协同作用。
Autophagy and multivesicular bodies (MVBs) represent 2 closely related lysosomal/vacuolar degradation pathways. In Arabidopsis (Arabidopsis thaliana), autophagy is stress-induced, with deficiency in autophagy causing strong defects in stress responses but limited effects on growth. LYST-INTERACTING PROTEIN 5 (LIP5) is a key regulator of stress-induced MVB biogenesis, and mutation ofLIP5also strongly compromises stress responses with little effect on growth in Arabidopsis. To determine the functional interactions of these 2 pathways in Arabidopsis, we generated mutations in both theLIP5andAUTOPHAGY-RELATED PROTEIN(ATG) genes.atg5/lip5andatg7/lip5double mutants displayed strong synergistic phenotypes in fitness characterized by stunted growth, early senescence, reduced survival, and greatly diminished seed production under normal growth conditions. Transcriptome and metabolite analysis revealed that chloroplast sulfate assimilation was specifically downregulated at early seedling stages in theatg7/lip5double mutant prior to the onset of visible phenotypes. Overexpression of adenosine 5′-phosphosulfate reductase 1, a key enzyme in sulfate assimilation, substantially improved the growth and fitness of theatg7/lip5double mutant. Comparative multi-omic analysis further revealed that theatg7/lip5double mutant was strongly compromised in other chloroplast functions including photosynthesis and primary carbon metabolism. Premature senescence and reduced survival ofatg/lip5double mutants were associated with increased accumulation of reactive oxygen species and overactivation of stress-associated programs. Blocking PHYTOALEXIN DEFICIENT 4 and salicylic acid signaling prevented early senescence and death of theatg7/lip5double mutant. Thus, stress-responsive autophagy and MVB pathways play an important cooperative role in protecting essential chloroplast functions including sulfur assimilation under normal growth conditions to suppress salicylic-acid-dependent premature cell-death and promote plant growth and fitness.