skip to main content


Title: Endoplasmic reticulum stress pathway mediates the early heat stress response of developing rice seeds
Abstract   more » « less
Award ID(s):
1736192
NSF-PAR ID:
10449201
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Plant, Cell & Environment
Volume:
44
Issue:
8
ISSN:
0140-7791
Page Range / eLocation ID:
p. 2604-2624
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Increasing global surface temperatures is posing a major food security challenge. Part of the solution to address this problem is to improve crop heat resilience, especially during grain development, along with agronomic decisions such as shift in planting time and increasing crop diversification. Rice is a major food crop consumed by more than 3 billion people. For rice, thermal sensitivity of reproductive development and grain filling is well‐documented, while knowledge concerning the impact of heat stress (HS) on early seed development is limited. Here, we aim to study the phenotypic variation in a set of diverse rice accessions for elucidating the HS response during early seed development. To explore the variation in HS sensitivity, we investigatedaus(1),indica(2), temperate japonica(2), and tropical japonica(4) accessions for their HS (39/35°C) response during early seed development that accounts for transition of endosperm from syncytial to cellularization, which broadly corresponds to 24 and 96 hr after fertilization (HAF), respectively, in rice. The twoindicaand one of thetropical japonicaaccessions exhibited severe heat sensitivity with increased seed abortion; threetropical japonicasand anausaccession showed moderate heat tolerance, whiletemperate japonicasexhibited strong heat tolerance. The accessions exhibiting extreme heat sensitivity maintain seed size at the expense of number of fully developed mature seeds, while the accessions showing relative resilience to the transient HS maintained number of fully developed seeds but compromised on seed size, especially seed length. Further, histochemical analysis revealed that all the tested accessions have delayed endosperm cellularization upon exposure to the transient HS by 96 HAF; however, the rate of cellularization was different among the accessions. These findings were further corroborated by upregulation of cellularization‐associated marker genes in the developing seeds from the heat‐stressed samples.

     
    more » « less
  2. Abstract

    Due to global climate change, heat stress is increasingly harming the growth, development, overall biomass, and grain yield of numerous crops. Heat stress impairs pollen development and thus reduces seed set inSorghum bicolor(L.) Moench; however, the effects of heat stress on anther development at specific stages and tiller formation remain incompletely understood. Here we report that exposure to heat stress [42°C/32°C (day/night)] at pollen mother cell (PMC) and booting stages profoundly disrupts tapetum and pollen development, resulting in a significant decrease in grain yield in sorghum. Sorghum plants subjected to 9 days or less of heat stress at the PMC stage exhibited normal pollen viability, but 12 days of heat stress caused almost complete loss of grain yield and the formation of nonviable pollen grains. Similarly, sorghum plants that were heat‐stressed for 3 days at the booting stage produced few seeds. Further analysis revealed that aberrant tapetum and pollen development contributed to the sterility of pollen in these heat‐stressed plants. Notably, in addition to inhibiting plant height, a 12‐day heat stress at the PMC stage promoted the formation of basal tillers, whereas a 3‐day heat stress at the booting stage stimulated the formation of apical tillers, which helped salvage seed yield under heat stress conditions. Moreover, the application of exogenous auxin promoted the formation of apical tillers and leaf numbers per apical tiller. Collectively, our findings suggest that sorghum is susceptible to heat stress during both early and late anther development, and auxin might be involved in governing the formation of apical tillers.

     
    more » « less
  3. Abstract Background

    The maize inbred line A188 is an attractive model for elucidation of gene function and improvement due to its high embryogenic capacity and many contrasting traits to the first maize reference genome, B73, and other elite lines. The lack of a genome assembly of A188 limits its use as a model for functional studies.

    Results

    Here, we present a chromosome-level genome assembly of A188 using long reads and optical maps. Comparison of A188 with B73 using both whole-genome alignments and read depths from sequencing reads identify approximately 1.1 Gb of syntenic sequences as well as extensive structural variation, including a 1.8-Mb duplication containing the Gametophyte factor1 locus for unilateral cross-incompatibility, and six inversions of 0.7 Mb or greater. Increased copy number of carotenoid cleavage dioxygenase 1 (ccd1) in A188 is associated with elevated expression during seed development. Highccd1expression in seeds together with low expression of yellow endosperm 1 (y1) reduces carotenoid accumulation, accounting for the white seed phenotype of A188. Furthermore, transcriptome and epigenome analyses reveal enhanced expression of defense pathways and altered DNA methylation patterns of the embryonic callus.

    Conclusions

    The A188 genome assembly provides a high-resolution sequence for a complex genome species and a foundational resource for analyses of genome variation and gene function in maize. The genome, in comparison to B73, contains extensive intra-species structural variations and other genetic differences. Expression and network analyses identify discrete profiles for embryonic callus and other tissues.

     
    more » « less
  4. Abstract

    Plants are increasingly exposed to high temperatures, which can cause accumulation of unfolded protein in the endoplasmic reticulum (ER). This condition, known as ER stress, evokes the unfolded protein response (UPR), a cytoprotective signaling pathway. One important branch of the UPR is regulated by splicing of bZIP60 mRNA by the IRE1 stress sensor. There is increasing evidence that commercial plant growth regulators may protect against abiotic stressors including heat stress and drought, but there is very little mechanistic information about these effects or about the regulatory pathways involved. We evaluated evidence in the B73 Zea mays inbred for differences in the activity of the UPR between permissive and elevated temperature in conjunction with plant growth regulator application. Treatment with elevated temperature and plant growth regulators increased UPR activation, as assessed by an increase in splicing of the mRNA of the IRE1 target bZIP60 following paclobutrazol treatment. We propose that plant growth regulator treatment induces bZIP60 mRNA splicing which ‘primes’ plants for rapid adaptive response to subsequent endoplasmic reticulum-stress inducing conditions.

     
    more » « less
  5. Abstract Background

    H2A.X is an H2A variant histone in eukaryotes, unique for its ability to respond to DNA damage, initiating the DNA repair pathway. H2A.X replacement within the histone octamer is mediated by the FAcilitates Chromatin Transactions (FACT) complex, a key chromatin remodeler. FACT is required for DEMETER (DME)-mediated DNA demethylation at certain loci inArabidopsis thalianafemale gametophytes during reproduction. Here, we sought to investigate whether H2A.X is involved in DME- and FACT-mediated DNA demethylation during reproduction.

    Results

    H2A.X is encoded by two genes in Arabidopsis genome,HTA3andHTA5. We generatedh2a.xdouble mutants, which displayed a normal growth profile, whereby flowering time, seed development, and root tip organization, S-phase progression and proliferation were all normal. However,h2a.xmutants were more sensitive to genotoxic stress, consistent with previous reports. H2A.X fused to Green Fluorescent Protein (GFP) under theH2A.Xpromoter was highly expressed especially in newly developing Arabidopsis tissues, including in male and female gametophytes, where DME is also expressed. We examined DNA methylation inh2a.xdeveloping seeds and seedlings using whole genome bisulfite sequencing, and found that CG DNA methylation is decreased genome-wide inh2a.xmutant endosperm. Hypomethylation was most striking in transposon bodies, and occurred on both parental alleles in the developing endosperm, but not the embryo or seedling.h2a.x-mediated hypomethylated sites overlapped DME targets, but also included other loci, predominately located in heterochromatic transposons and intergenic DNA.

    Conclusions

    Our genome-wide methylation analyses suggest that H2A.X could function in preventing access of the DME demethylase to non-canonical sites. Overall, our data suggest that H2A.X is required to maintain DNA methylation homeostasis in the unique chromatin environment of the Arabidopsis endosperm.

     
    more » « less