Sexual reproduction in plants requires development of haploid gametophytes from somatic tissues. Pollen is the male gametophyte and develops within the stamen; defects in the somatic tissues of the stamen and in the male gametophyte itself can result in male sterility. The maize fuzzy tassel (fzt) mutant has a mutation in dicer-like1 (dcl1), which encodes a key enzyme required for microRNA (miRNA) biogenesis. Many miRNAs are reduced in fzt, and fzt mutants exhibit a broad range of developmental defects, including male sterility. To gain further insight into the roles of miRNAs in maize stamen development, we conducted a detailed analysis of the male sterility defects in fzt mutants. Early development was normal in fzt mutant anthers, however fzt anthers arrested in late stages of anther maturation and did not dehisce. A minority of locules in fzt anthers also exhibited anther wall defects. At maturity, very little pollen in fzt anthers was viable or able to germinate. Normal pollen is tricellular at maturity; pollen from fzt anthers included a mixture of unicellular, bicellular, and tricellular pollen. Pollen from normal anthers is loaded with starch before dehiscence, however pollen from fzt anthers failed to accumulate starch. Our results indicate an absolute requirement for miRNAs in the final stages of anther and pollen maturation in maize. Anther wall defects also suggest that miRNAs have key roles earlier in anther development. We discuss candidate miRNAs and pathways that might underlie fzt anther defects, and also note that male sterility in fzt resembles water deficit-induced male sterility, highlighting a possible link between development and stress responses in plants.
This review highlights recent literature on biomolecular condensates in plant development and discusses challenges for fully dissecting their functional roles. Plant developmental biology has been inundated with descriptive examples of biomolecular condensate formation, but it is only recently that mechanistic understanding has been forthcoming. Here, we discuss recent examples based on current findings in plant and cell biology at different stages of the plant life cycle. We group these examples based on putative molecular functions, including: sequestering interacting components, enhancing dwell time, and interacting with cytoplasmic biophysical properties in response to environmental change. We explore how these mechanisms modulate plant development in response to environmental inputs and discuss challenges and opportunities for further research into deciphering molecular mechanisms to better understand the diverse roles that biomolecular condensates exert on life.
During the energy crisis associated with submergence stress, plants restrict mRNA translation and rapidly accumulate stress granules that act as storage hubs for arrested mRNA complexes. One of the proteins associated with hypoxia-induced stress granules in Arabidopsis thaliana is the calcium-sensor protein CALMODULIN-LIKE 38 (CML38). Here, we show that SUPPRESSOR OF GENE SILENCING 3 (SGS3) is a CML38-binding protein, and that SGS3 and CML38 co-localize within hypoxia-induced RNA stress granule-like structures. Hypoxia-induced SGS3 granules are subject to turnover by autophagy, and this requires both CML38 as well as the AAA+-ATPase CELL DIVISION CYCLE 48A (CDC48A). CML38 also interacts directly with CDC48A, and CML38 recruits CDC48A to CML38 granules in planta. Together, this work demonstrates that SGS3 associates with stress granule-like structures during hypoxia stress that are subject to degradation by CML38 and CDC48-dependent autophagy. Further, the work identifies direct regulatory targets for the hypoxia calcium-sensor CML38, and suggest that CML38 association with stress granules and associated regulation of autophagy may be part of the RNA regulatory program during hypoxia stress.
In response to the energy crisis resulting from submergence stress and hypoxia, Arabidopsis limits non-essential mRNAs translation, and accumulate cytosolic stress granules (SG). SGs are phase-separated mRNA-protein particles that partition transcripts for various fates: storage, degradation, or return to translation after stress alleviation. Here, it is shown that RNA stress granules are dynamically regulated during hypoxia stress and aerobic recovery via two phases of autophagy that require the AAA+ ATPase CDC48 and the calcium sensor Calmodulin-like 38 (CML38). CML38 is a core hypoxia response-protein that associates with hypoxia-induced SGs. We show that CML38 is essential for SG autophagy during extended hypoxia. Further, cml38 mutants show disorganized SG morphology during extended hypoxia, suggesting a role in SG formation and maintenance. We also show that upon the return of aerobic conditions, intracellular calcium and CML38 are necessary for SG breakdown and turnover, and for upregulating autophagy. cml38 mutants not only lose these responses, but also have aberrant, sustained autophagosome accumulation during the reoxygenation recovery phase. The findings suggest that CDC48 RNA granule autophagy (“granulophagy”) is conserved in plants, and that the hypoxia-induced calcium sensor CML38 regulates SG autophagy during anaerobic stress as well as during the reprogramming phase associated with reoxygenation.
Heat waves, now more frequent and longer due to climate change, devastate plant productivity. Although rare, thermophilic plants could hold keys to engineering heat resilience in crop plants. Tidestromia oblongifolia is a thermophilic flowering plant that thrives at temperatures above 45C. When exposed to Death Valley summer conditions, T. oblongifolia increased its thermal optimum of photosynthesis within a day and accelerated growth within 10 days. The physiological changes were accompanied by morphological, anatomical, and gene expression changes revealed by a newly sequenced genome. In bundle sheath cells where Rubisco fixes CO2, mitochondria relocated to chloroplasts and novel, cup-shaped chloroplasts appeared. Understanding how this plant acclimates under heat may afford new ways of engineering heat tolerance in crop plants.
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