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HOS1 ubiquitinates SPL9 for degradation to modulate salinity-delayed flowering
Zhixin Jiao, Xiaoning Shi, Rui Xu, Mingxia Zhang, Leelyn Chong, Yingfang Zhu
J Integr Plant Biol 2024, 66 (12): 2600-2612.
DOI:
10.1111/jipb.13784
Abstract
(Browse
115
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Soil salinity is a serious environmental threat to plant growth and flowering. Flowering in the right place, at the right time, ensures maximal reproductive success for plants. Salinity-delayed flowering is considered a stress coping/survival strategy and the molecular mechanisms underlying this process require further studies to enhance the crop's salt tolerance ability. A nuclear pore complex (NPC) component, HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENE 1 (HOS1), has been recognized as a negative regulator of plant cold responses and flowering. Here, we challenged the role of HOS1 in regulating flowering in response to salinity stress. Interestingly, we discovered that HOS1 can directly interact with and ubiquitinate transcription factor SPL9 (SQUAMOSA PROMOTER BINDING PROTEIN-LIKE 9) to promote its protein degradation in response to salinity stress. Moreover, we demonstrated that
HOS1
and
SPL9
antagonistically regulate plant flowering under both normal and salt stress conditions. HOS1 was further shown to negatively regulate the expression of
SPLs
and several key flowering genes in response to salinity stress. These results jointly revealed that HOS1 is an important integrator in the process of modulating salinity-delayed flowering, thus offering new perspectives on a salinity stress coping strategy of plants.
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The
LpHsfA2
-molecular module confers thermotolerance via fine tuning of its transcription in perennial ryegrass (
Lolium perenne
L.)
Guangjing Ma, Zhihao Liu, Shurui Song, Jing Gao, Shujie Liao, Shilong Cao, Yan Xie, Liwen Cao, Longxing Hu, Haichun Jing, Liang Chen
J Integr Plant Biol 2024, 66 (11): 2346-2361.
doi:
10.1111/jipb.13789
Abstract
(Browse
77
) |
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Temperature sensitivity and tolerance play a key role in plant survival and production. Perennial ryegrass (
Lolium perenne
L.), widely cultivated in cool-season for forage supply and turfgrass, is extremely susceptible to high temperatures, therefore serving as an excellent grass for dissecting the genomic and genetic basis of high-temperature adaptation. In this study, expression analysis revealed that
LpHsfA2
, an important gene associated with high-temperature tolerance in perennial ryegrass, is rapidly and substantially induced under heat stress. Additionally, heat-tolerant varieties consistently display elevated expression levels of
LpHsfA2
compared with heat-sensitive ones. Comparative haplotype analysis of the
LpHsfA2
promoter indicated an uneven distribution of two haplotypes (
HsfA2
Hap1
and
HsfA2
Hap2
) across varieties with differing heat tolerance. Specifically, the
HsfA2
Hap1
allele is predominantly present in heat-tolerant varieties, while the
HsfA2
Hap2
allele exhibits the opposite pattern. Overexpression of
LpHsfA2
confers enhanced thermotolerance, whereas silencing of
LpHsfA2
compromises heat tolerance. Furthermore,
LpHsfA2
orchestrates its protective effects by directly binding to the promoters of
LpHSP18
.2 and
LpAPX1
to activate their expression, preventing the non-specific misfolding of intracellular protein and the accumulation of reactive oxygen species in cells. Additionally, LpHsfA4 and LpHsfA5 were shown to engage directly with the promoter of
LpHsfA2
, upregulating its expression as well as the expression of
LpHSP18
.2 and
LpAPX1
, thus contributing to enhanced heat tolerance. Markedly, LpHsfA2 possesses autoregulatory ability by directly binding to its own promoter to modulate the self-transcription. Based on these findings, we propose a model for modulating the thermotolerance of perennial ryegrass by precisely regulating the expression of LpHsfA2. Collectively, these findings provide a scientific basis for the development of thermotolerant perennial ryegrass cultivars.
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Simultaneous mutations in
ITPK4
and
MRP5
genes result in a low phytic acid level without compromising salt tolerance in
Arabidopsis
Yuying Ren, Mengdan Jiang, Jian-Kang Zhu, Wenkun Zhou, Chunzhao Zhao
J Integr Plant Biol 2024, 66 (10): 2109-2125.
DOI:
10.1111/jipb.13745
Abstract
(Browse
138
) |
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Generation of crops with low phytic acid (
myo
-inositol-1,2,3,4,5,6-hexakisphosphate (InsP
6
)) is an important breeding direction, but such plants often display less desirable agronomic traits. In this study, through ethyl methanesulfonate-mediated mutagenesis, we found that inositol 1,3,4-trisphosphate 5/6-kinase 4 (ITPK4), which is essential for producing InsP
6
, is a critical regulator of salt tolerance in
Arabidopsis
. Loss of function of
ITPK4
gene leads to reduced root elongation under salt stress, which is primarily because of decreased root meristem length and reduced meristematic cell number. The
itpk4
mutation also results in increased root hair density and increased accumulation of reactive oxygen species during salt exposure. RNA sequencing assay reveals that several auxin-responsive genes are down-regulated in the
itpk4-1
mutant compared to the wild-type. Consistently, the
itpk4-1
mutant exhibits a reduced auxin level in the root tip and displays compromised gravity response, indicating that ITPK4 is involved in the regulation of the auxin signaling pathway. Through suppressor screening, it was found that mutation of
Multidrug Resistance Protein 5 (MRP5)5
gene, which encodes an ATP-binding cassette (ABC) transporter required for transporting InsP
6
from the cytoplasm into the vacuole, fully rescues the salt hypersensitivity of the
itpk4-1
mutant, but in the
itpk4-1
mrp5
double mutant, InsP
6
remains at a very low level. These results imply that InsP
6
homeostasis rather than its overall amount is beneficial for stress tolerance in plants. Collectively, this study uncovers a pair of gene mutations that confer low InsP
6
content without impacting stress tolerance, which offers a new strategy for creating “low-phytate” crops.
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STOP1 regulates CCX1-mediated Ca
2+
homeostasis for plant adaptation to Ca
2+
deprivation
Wen Hao Tian, Wen Yan Cai, Chun Quan Zhu, Ya Li Kong, Xiao Chuang Cao, Lian Feng Zhu, Jia Yuan Ye, Jun Hua Zhang, Shao Jian Zheng
J Integr Plant Biol 2024, 66 (10): 2126-2139.
DOI:
10.1111/jipb.13754
Abstract
(Browse
80
) |
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Calcium (Ca) is essential for plant growth and stress adaptation, yet its availability is often limited in acidic soils, posing a major threat to crop production. Understanding the intricate mechanisms orchestrating plant adaptation to Ca deficiency remains elusive. Here, we show that the Ca deficiency-enhanced nuclear accumulation of the transcription factor SENSITIVE TO PROTON RHIZOTOXICITY 1 (STOP1) in
Arabidopsis thaliana
confers tolerance to Ca deprivation, with the global transcriptional responses triggered by Ca deprivation largely impaired in the
stop1
mutant. Notably, STOP1 activates the Ca deprivation-induced expression of
CATION/Ca
2+
EXCHANGER 1 (CCX1)
by directly binding to its promoter region, which facilitates Ca
2+
efflux from endoplasmic reticulum to cytosol to maintain Ca homeostasis. Consequently, the constitutive expression of
CCX1
in the
stop1
mutant partially rescues the Ca deficiency phenotype by increasing Ca content in the shoots. These findings uncover the pivotal role of the STOP1-CCX1 axis in plant adaptation to low Ca, offering alternative manipulating strategies to improve plant Ca nutrition in acidic soils and extending our understanding of the multifaceted role of STOP1.
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The combination of a microbial and a non-microbial biostimulant increases yield in lettuce (
Lactuca sativa
) under salt stress conditions by up-regulating cytokinin biosynthesis
Patricia Benito, Marina Celdrán, Javier Bellón, Vicente Arbona, Miguel González-Guzmán, Rosa Porcel, Lynne Yenush, José M. Mulet
J Integr Plant Biol 2024, 66 (10): 2140-2157.
doi:
10.1111/jipb.13755
Abstract
(Browse
86
) |
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Salinization poses a significant challenge in agriculture, exacerbated by anthropogenic global warming. Biostimulants, derived from living microorganisms or natural extracts, have emerged as valuable tools for conventional and organic agriculture. However, our understanding of the molecular mechanisms underlying the effects of biostimulants is very limited, especially in crops under real cultivation conditions. In this study, we adopted an integrative approach to investigate the effectiveness of the combined application of plant growth-promoting bacterium (
Bacillus megaterium
strain BM08) and a non-microbial biostimulant under control conditions (normal watering) and salt stress. After confirming the yield increase under both conditions, we investigated the molecular mechanisms underlying the observed effect by measuring a number of physiological parameters (i.e., lipid peroxidation, antioxidants, chlorophylls, total phenolics and phytohormone content), as well as RNA sequencing and primary metabolite analyses. Our findings reveal that the combined effect of the microbial and non-microbial biostimulants led to a decrease in the antioxidant response and an up-regulation of genes involved in cytokinin biosynthesis under salt stress conditions. This, in turn, resulted in a higher concentration of the bioactive cytokinin, isopentenyladenosine, in roots and leaves and an increase in γ-aminobutyric acid, a non-proteic amino acid related to abiotic stress responses. In addition, we observed a decrease in malic acid, along with an abscisic acid (ABA)-independent up-regulation of SR-kinases, a family of protein kinases associated with abiotic stress responses. Furthermore, we observed that the single application of the non-microbial biostimulant triggers an ABA-dependent response under salt stress; however, when combined with the microbial biostimulant, it potentiated the mechanisms triggered by the BM08 bacterial strain. This comprehensive investigation shows that the combination of two biostimulants is able to elicit a cytokinin-dependent response that may explain the observed yield increase under salt stress conditions.
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Maize ZmSRO1e promotes mesocotyl elongation and deep sowing tolerance by inhibiting the activity of ZmbZIP61
Lumin Qin, Fangfang Kong, Lin Wei, Minghan Cui, Jianhang Li, Chen Zhu, Yue Liu, Guangmin Xia, Shuwei Liu
J Integr Plant Biol 2024, 66 (8): 1571-1586.
DOI:
10.1111/jipb.13714
Abstract
(Browse
104
) |
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Deep sowing is a traditional method for drought resistance in maize production, and mesocotyl elongation is strongly associated with the ability of maize to germinate from deep soil. However, little is known about the functional genes and mechanisms regulating maize mesocotyl elongation. In the present study, we identified a plant‐specific SIMILAR TO RCD‐ONE (SRO) protein family member, ZmSRO1e, involved in maize mesocotyl elongation. The expression of
ZmSRO1e
is strongly inhibited upon transfer from dark to white light. The loss‐of‐function
zmsro1e
mutant exhibited a dramatically shorter mesocotyl than the wild‐type in both constant light and darkness, while overexpression of
ZmSRO1e
significantly promoted mesocotyl elongation, indicating that ZmSRO1e positively regulates mesocotyl elongation. We showed that ZmSRO1e physically interacted with ZmbZIP61, an ortholog of Arabidopsis ELONGATED HYPOCOTYL 5 (HY5) and showed a function similar to that of HY5 in regulating photomorphogenesis. We found that ZmSRO1e repressed the transcriptional activity of ZmbZIP61 toward target genes involved in the regulation of cell expansion, such as
ZmEXPB4
and
ZmEXPB6
, by interfering with the binding of ZmbZIP61 to the promoters of target genes. Our results provide a new understanding of the mechanism by which SRO regulates photomorphogenesis and highlight its potential application in deep sowing‐resistant breeding.
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Overexpression of tonoplast Ca
2+
‐ATPase in guard cells synergistically enhances stomatal opening and drought tolerance
Jinghan Su, Bingqing He, Peiyuan Li, Baiyang Yu, Qiwen Cen, Lingfeng Xia, Yi Jing, Feibo Wu, Rucha Karnik, Dawei Xue, Michael R. Blatt and Yizhou Wang
J Integr Plant Biol 2024, 66 (8): 1587-1602.
DOI:
10.1111/jipb.13721
Abstract
(Browse
120
) |
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Stomata play a crucial role in plants by controlling water status and responding to drought stress. However, simultaneously improving stomatal opening and drought tolerance has proven to be a significant challenge. To address this issue, we employed the OnGuard quantitative model, which accurately represents the mechanics and coordination of ion transporters in guard cells. With the guidance of OnGuard, we successfully engineered plants that overexpressed the main tonoplast Ca
2+
‐ATPase gene,
ACA11
, which promotes stomatal opening and enhances plant growth. Surprisingly, these transgenic plants also exhibited improved drought tolerance due to reduced water loss through their stomata. Again, OnGuard assisted us in understanding the mechanism behind the unexpected stomatal behaviors observed in the
ACA11
overexpressing plants. Our study revealed that the overexpression of
ACA11
facilitated the accumulation of Ca
2+
in the vacuole, thereby influencing Ca
2+
storage and leading to an enhanced Ca
2+
elevation in response to abscisic acid. This regulatory cascade finely tunes stomatal responses, ultimately leading to enhanced drought tolerance. Our findings underscore the importance of tonoplast Ca
2+
‐ATPase in manipulating stomatal behavior and improving drought tolerance. Furthermore, these results highlight the diverse functions of tonoplast‐localized ACA11 in response to different conditions, emphasizing its potential for future applications in plant enhancement.
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Ca
2+
-independent ZmCPK2 is inhibited by Ca
2+
-dependent ZmCPK17 during drought response in maize
Xiaoying Hu, Jinkui Cheng, Minmin Lu, Tingting Fang, Yujuan Zhu, Zhen Li, Xiqing Wang, Yu Wang, Yan Guo, Shuhua Yang, Zhizhong Gong
J Integr Plant Biol 2024, 66 (7): 1313-1333.
DOI:
10.1111/jipb.13675
Abstract
(Browse
251
) |
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Calcium oscillations are induced by different stresses. Calcium-dependent protein kinases (CDPKs/CPKs) are one major group of the plant calcium decoders that are involved in various processes including drought response. Some CPKs are calcium-independent. Here, we identified ZmCPK2 as a negative regulator of drought resistance by screening an overexpression transgenic maize pool. We found that ZmCPK2 does not bind calcium, and its activity is mainly inhibited during short term abscisic acid (ABA) treatment, and dynamically changed in prolonged treatment. Interestingly, ZmCPK2 interacts with and is inhibited by calcium-dependent ZmCPK17, a positive regulator of drought resistance, which is activated by ABA. ZmCPK17 could prevent the nuclear localization of ZmCPK2 through phosphorylation of ZmCPK2T60. ZmCPK2 interacts with and phosphorylates and activates ZmYAB15, a negative transcriptional factor for drought resistance. Our results suggest that drought stress-induced Ca
2+
can be decoded directly by ZmCPK17 that inhibits ZmCPK2, thereby promoting plant adaptation to water deficit.
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Phosphorylation of ZmAL14 by ZmSnRK2.2 regulates drought resistance through derepressing
ZmROP8
expression
Yalin Wang, Jinkui Cheng, Yazhen Guo, Zhen Li, Shuhua Yang, Yu Wang, Zhizhong Gong
J Integr Plant Biol 2024, 66 (7): 1334-1350.
DOI:
10.1111/jipb.13677
Abstract
(Browse
140
) |
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Drought stress has negative effects on crop growth and production. Characterization of transcription factors that regulate the expression of drought-responsive genes is critical for understanding the transcriptional regulatory networks in response to drought, which facilitates the improvement of crop drought tolerance. Here, we identified an Alfin-like (AL) family gene
ZmAL14
that negatively regulates drought resistance. Overexpression of
ZmAL14
exhibits susceptibility to drought while mutation of
ZmAL14
enhances drought resistance. An abscisic acid (ABA)-activated protein kinase ZmSnRK2.2 interacts and phosphorylates ZmAL14 at T38 residue. Knockout of
ZmSnRK2.2
gene decreases drought resistance of maize. A dehydration-induced Rho-like small guanosine triphosphatase gene
ZmROP8
is directly targeted and repressed by ZmAL14. Phosphorylation of ZmAL14 by ZmSnRK2.2 prevents its binding to the
ZmROP8
promoter, thereby releasing the repression of
ZmROP8
transcription. Overexpression of
ZmROP8
stimulates peroxidase activity and reduces hydrogen peroxide accumulation after drought treatment. Collectively, our study indicates that ZmAL14 is a negative regulator of drought resistance, which can be phosphorylated by ZmSnRK2.2 through the ABA signaling pathway, thus preventing its suppression on
ZmROP8
transcription during drought stress response.
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ACBP4-WRKY70-
RAP2.12
module positively regulates submergence-induced hypoxia response in
Arabidopsis thaliana
Mengyun Guo, Yingjun Yao, Kangqun Yin, Luna Tan, Meng Liu, Jing Hou, Han Zhang, Ruyun Liang, Xinran Zhang, Heng Yang, Xiaoxiao Chen, Jinrui Tan, Yan Song, Shangling Lou, Liyang Chen, Xuejing Liu, Si Tang, Yongqi Hu, Jin Yan, Wensen Fu, Kai Yang, Ruijia Zhang, Xuerui Li, Yao Liu, Zhen Yan, Wei Liu, Yu Han, Jianquan Liu, Kangshan Mao and Huanhuan Liu
J Integr Plant Biol 2024, 66 (6): 1052-1067.
doi:
10.1111/jipb.13647
Abstract
(Browse
152
) |
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ACYL-CoA-BINDING PROTEINs (ACBPs) play crucial regulatory roles during plant response to hypoxia, but their molecular mechanisms remain poorly understood. Our study reveals that ACBP4 serves as a positive regulator of the plant hypoxia response by interacting with WRKY70, influencing its nucleocytoplasmic shuttling in
Arabidopsis thaliana
. Furthermore, we demonstrate the direct binding of WRKY70 to the
ACBP4
promoter, resulting in its upregulation and suggesting a positive feedback loop. Additionally, we pinpointed a phosphorylation site at Ser638 of ACBP4, which enhances submergence tolerance, potentially by facilitating WRKY70′s nuclear shuttling. Surprisingly, a natural variation in this phosphorylation site of ACBP4 allowed
A. thaliana
to adapt to humid conditions during its historical demographic expansion. We further observed that both phosphorylated ACBP4 and oleoyl-CoA can impede the interaction between ACBP4 and WRKY70, thus promoting WRKY70's nuclear translocation. Finally, we found that the overexpression of orthologous
BnaC5.ACBP4
and
BnaA7.WRKY70
in Brassica napus increases submergence tolerance, indicating their functional similarity across genera. In summary, our research not only sheds light on the functional significance of the
ACBP4
gene in hypoxia response, but also underscores its potential utility in breeding flooding-tolerant oilseed rape varieties.
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Autophagy receptor ZmNBR1 promotes the autophagic degradation of ZmBRI1a and enhances drought tolerance in maize
Yang Xiang, Guangdong Li, Qian Li, Yingxue Niu, Yitian Pan, Yuan Cheng, Xiangli Bian, Chongyang Zhao, Yuanhong Wang and Aying Zhang
J Integr Plant Biol 2024, 66 (6): 1068-1086.
DOI:
10.1111/jipb.13662
Abstract
(Browse
120
) |
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Drought stress is a crucial environmental factor that limits plant growth, development, and productivity. Autophagy of misfolded proteins can help alleviate the damage caused in plants experiencing drought. However, the mechanism of autophagy-mediated drought tolerance in plants remains largely unknown. Here, we cloned the gene for a maize (
Zea mays
) selective autophagy receptor,
NEXT TO BRCA1 GENE 1
(
ZmNBR1
), and identified its role in the response to drought stress. We observed that drought stress increased the accumulation of autophagosomes. RNA sequencing and reverse transcription-quantitative polymerase chain reaction showed that
ZmNBR1
is markedly induced by drought stress.
ZmNBR1
overexpression enhanced drought tolerance, while its knockdown reduced drought tolerance in maize. Our results established that
ZmNBR1
mediates the increase in autophagosomes and autophagic activity under drought stress. ZmNBR1 also affects the expression of genes related to autophagy under drought stress. Moreover, we determined that BRASSINOSTEROID INSENSITIVE 1A (ZmBRI1a), a brassinosteroid receptor of the BRI1-like family, interacts with ZmNBR1. Phenotype analysis showed that ZmBRI1a negatively regulates drought tolerance in maize, and genetic analysis indicated that ZmNBR1 acts upstream of ZmBRI1a in regulating drought tolerance. Furthermore, ZmNBR1 facilitates the autophagic degradation of ZmBRI1a under drought stress. Taken together, our results reveal that ZmNBR1 regulates the expression of autophagy-related genes, thereby increasing autophagic activity and promoting the autophagic degradation of ZmBRI1a under drought stress, thus enhancing drought tolerance in maize. These findings provide new insights into the autophagy degradation of brassinosteroid signaling components by the autophagy receptor NBR1 under drought stress.
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UVR8-TCP4-LOX2 module regulates UV-B tolerance in Arabidopsis
Cheng Li, Jiancan Du, Huini Xu, Zhenhua Feng, Caspar C. C. Chater, Yuanwen Duan, Yongping Yang and Xudong Sun
J Integr Plant Biol 2024, 66 (5): 897-908.
doi:
10.1111/jipb.13648
Abstract
(Browse
128
) |
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The phytohormone jasmonate (JA) coordinates stress and growth responses to increase plant survival in unfavorable environments. Although JA can enhance plant UV-B stress tolerance, the mechanisms underlying the interaction of UV-B and JA in this response remain unknown. In this study, we demonstrate that the UV RESISTANCE LOCUS 8 - TEOSINTE BRANCHED1, Cycloidea and PCF 4 - LIPOXYGENASE2 (UVR8-TCP4-LOX2) module regulates UV-B tolerance dependent on JA signaling pathway in
Arabidopsis thaliana
. We show that the nucleus-localized UVR8 physically interacts with TCP4 to increase the DNA-binding activity of TCP4 and upregulate the JA biosynthesis gene
LOX2
. Furthermore, UVR8 activates the expression of
LOX2
in a TCP4-dependent manner. Our genetic analysis also provides evidence that TCP4 acts downstream of UVR8 and upstream of
LOX2
to mediate plant responses to UV-B stress. Our results illustrate that the UV-B-dependent interaction of UVR8 and TCP4 serves as an important UVR8-TCP4-LOX2 module, which integrates UV-B radiation and JA signaling and represents a new UVR8 signaling mechanism in plants.
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TabHLH27 orchestrates root growth and drought tolerance to enhance water use efficiency in wheat
Dongzhi Wang, Xiuxiu Zhang, Yuan Cao, Aamana Batool, Yongxin Xu, Yunzhou Qiao, Yongpeng Li, Hao Wang, Xuelei Lin, Xiaomin Bie, Xiansheng Zhang, Ruilian Jing, Baodi Dong, Yiping Tong, Wan Teng, Xigang Liu, Jun Xiao
J Integr Plant Biol 2024, 66 (7): 1295-1312.
DOI:
10.1111/jipb.13670
Abstract
(Browse
208
) |
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Cultivating high-yield wheat under limited water resources is crucial for sustainable agriculture in semiarid regions. Amid water scarcity, plants activate drought response signaling, yet the delicate balance between drought tolerance and development remains unclear. Through genome-wide association studies and transcriptome profiling, we identified a wheat atypical basic helix-loop-helix (bHLH) transcription factor (TF), TabHLH27-A1, as a promising quantitative trait locus candidate for both relative root dry weight and spikelet number per spike in wheat. TabHLH27-A1/B1/D1 knock-out reduced wheat drought tolerance, yield, and water use efficiency (WUE).
TabHLH27-A1
exhibited rapid induction with polyethylene glycol (PEG) treatment, gradually declining over days. It activated stress response genes such as
TaCBL8-B1
and
TaCPI2-A1
while inhibiting root growth genes like
TaSH15-B1
and
TaWRKY70-B1
under short-term PEG stimulus. The distinct transcriptional regulation of TabHLH27-A1 involved diverse interacting factors such as TaABI3-D1 and TabZIP62-D1. Natural variations of
TabHLH27-A
1 influence its transcriptional responses to drought stress, with
TabHLH27-A1
Hap-II
associated with stronger drought tolerance, larger root system, more spikelets, and higher WUE in wheat. Significantly, the excellent
TabHLH27-A1
Hap-II
was selected during the breeding process in China, and introgression of
TabHLH27-A1
Hap-II
allele improved drought tolerance and grain yield, especially under water-limited conditions. Our study highlights TabHLH27-A1's role in balancing root growth and drought tolerance, providing a genetic manipulation locus for enhancing WUE in wheat.
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OsNAC5 orchestrates OsABI5 to fine-tune cold tolerance in rice
Ruiqing Li, Yue Song, Xueqiang Wang, Chenfan Zheng, Bo Liu, Huali Zhang, Jian Ke, Xuejing Wu, Liquan Wu, Ruifang Yang and Meng Jiang
J Integr Plant Biol 2024, 66 (4): 660-682.
DOI:
10.1111/jipb.13585
Abstract
(Browse
374
) |
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Due to its tropical origins, rice (
Oryza sativa
) is susceptible to cold stress, which poses severe threats to production. OsNAC5, a NAC-type transcription factor, participates in the cold stress response of rice, but the detailed mechanisms remain poorly understood. Here, we demonstrate that OsNAC5 positively regulates cold tolerance at germination and in seedlings by directly activating the expression of
ABSCISIC ACID INSENSITIVE 5
(
OsABI5
). Haplotype analysis indicated that single nucleotide polymorphisms in a NAC-binding site in the
OsABI5
promoter are strongly associated with cold tolerance. OsNAC5 also enhanced OsABI5 stability, thus regulating the expression of cold-responsive (
COR
) genes, enabling fine-tuned control of OsABI5 action for rapid, precise plant responses to cold stress. DNA affinity purification sequencing coupled with transcriptome deep sequencing identified several OsABI5 target genes involved in
COR
expression, including
DEHYDRATION-RESPONSIVE ELEMENT BINDING FACTOR 1A
(
OsDREB1A
),
OsMYB20
, and
PEROXIDASE 70
(
OsPRX70
).
In vivo
and
in vitro
analyses suggested that OsABI5 positively regulates
COR
gene transcription, with marked
COR
upregulation in
OsNAC5
-overexpressing lines and downregulation in
osnac5
and/or
osabi5
knockout mutants. This study extends our understanding of cold tolerance regulation via OsNAC5 through the OsABI5-
COR
s transcription module, which may be used to ameliorate cold tolerance in rice via advanced breeding.
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An alfalfa MYB-like transcriptional factor MsMYBH positively regulates alfalfa seedling drought resistance and undergoes MsWAV3-mediated degradation
Kun Shi, Jia Liu, Huan Liang, Hongbin Dong, Jinli Zhang, Yuanhong Wei, Le Zhou, Shaopeng Wang, Jiahao Zhu, Mingshu Cao, Chris S. Jones, Dongmei Ma and Zan Wang
J Integr Plant Biol 2024, 66 (4): 683-699.
doi:
10.1111/jipb.13626
Abstract
(Browse
214
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Drought is a major threat to alfalfa (
Medicago sativa
L.) production. The discovery of important alfalfa genes regulating drought response will facilitate breeding for drought-resistant alfalfa cultivars. Here, we report a genome-wide association study of drought resistance in alfalfa. We identified and functionally characterized an MYB-like transcription factor gene (
MsMYBH
), which increases the drought resistance in alfalfa. Compared with the wild-types, the biomass and forage quality were enhanced in
MsMYBH
overexpressed plants. Combined RNA-seq, proteomics and chromatin immunoprecipitation analysis showed that MsMYBH can directly bind to the promoters of
MsMCP1, MsMCP2, MsPRX1A
and
MsCARCAB
to improve their expression. The outcomes of such interactions include better water balance, high photosynthetic efficiency and scavenge excess H
2
O
2
in response to drought. Furthermore, an E3 ubiquitin ligase (MsWAV3) was found to induce MsMYBH degradation under long-term drought, via the 26S proteasome pathway. Furthermore, variable-number tandem repeats in
MsMYBH
promoter were characterized among a collection of germplasms, and the variation is associated with promoter activity. Collectively, our findings shed light on the functions of
MsMYBH
and provide a pivotal gene that could be leveraged for breeding drought-resistant alfalfa. This discovery also offers new insights into the mechanisms of drought resistance in alfalfa.
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Structural insights into the
Oryza sativa
cation transporters HKTs in salt tolerance
Ran Gao, Yutian Jia, Xia Xu, Peng Fu, Jiaqi Zhou and Guanghui Yang
J Integr Plant Biol 2024, 66 (4): 700-708.
DOI:
10.1111/jipb.13632
Abstract
(Browse
105
) |
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The high-affinity potassium transporters (HKTs), selectively permeable to either Na
+
alone or Na
+
/K
+
, play pivotal roles in maintaining plant Na
+
/K
+
homeostasis. Although their involvement in salt tolerance is widely reported, the molecular underpinnings of
Oryza sativa
HKTs remain elusive. In this study, we elucidate the structures of OsHKT1;1 and OsHKT2;1, representing two distinct classes of rice HKTs. The dimeric assembled OsHKTs can be structurally divided into four domains. At the dimer interface, a half-helix or a loop in the third domain is coordinated by the C-terminal region of the opposite subunit. Additionally, we present the structures of OsHKT1;5 salt-tolerant and salt-sensitive variants, a key quantitative trait locus associated with salt tolerance. The salt-tolerant variant of OsHKT1;5 exhibits enhanced Na
+
transport capability and displays a more flexible conformation. These findings shed light on the molecular basis of rice HKTs and provide insights into their role in salt tolerance.
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The OsWRKY72-OsAAT30/OsGSTU26 module mediates reactive oxygen species scavenging to drive heterosis for salt tolerance in hybrid rice
Citao Liu, Bigang Mao, Yanxia Zhang, Lei tian, Biao Ma, Zhuo Chen, Zhongwei Wei, Aifu Li, Ye Shao, Gongye Cheng, Lingling Li, Wenyu Li, Di Zhang, Xiaoping Ding, Jiangxiang Peng, Yulin Peng, Jiwai He, Nenghui Ye, Dingyang Yuan, Chengcai Chu and Meijuan Duan
J Integr Plant Biol 2024, 66 (4): 709-730.
DOI:
10.1111/jipb.13640
Abstract
(Browse
171
) |
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Hybrid rice (
Oryza sativa
) generally outperforms its inbred parents in yield and stress tolerance, a phenomenon termed heterosis, but the underlying mechanism is not completely understood. Here, we combined transcriptome, proteome, physiological, and heterosis analyses to examine the salt response of super hybrid rice Chaoyou1000 (CY1000). In addition to surpassing the mean values for its two parents (mid-parent heterosis), CY1000 exhibited a higher reactive oxygen species scavenging ability than both its parents (over-parent heterosis or heterobeltiosis). Nonadditive expression and allele-specific gene expression assays showed that the glutathione S-transferase gene
OsGSTU26
and the amino acid transporter gene
OsAAT30
may have major roles in heterosis for salt tolerance, acting in an overdominant fashion in CY1000. Furthermore, we identified OsWRKY72 as a common transcription factor that binds and regulates
OsGSTU26
and
OsAAT30
. The salt-sensitive phenotypes were associated with the
OsWRKY72
paternal
genotype or the
OsAAT30
maternal
genotype in core rice germplasm varieties. OsWRKY72
paternal
specifically repressed the expression of
OsGSTU26
under salt stress, leading to salinity sensitivity, while OsWRKY72
maternal
specifically repressed
OsAAT30
, resulting in salinity tolerance. These results suggest that the OsWRKY72-OsAAT30/OsGSTU26 module may play an important role in heterosis for salt tolerance in an overdominant fashion in CY1000 hybrid rice, providing valuable clues to elucidate the mechanism of heterosis for salinity tolerance in hybrid rice.
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Potassium transporter OsHAK9 regulates seed germination under salt stress by preventing gibberellin degradation through mediating
OsGA2ox7
in rice
Peng Zeng, Ting Xie, Jiaxin Shen, Taokai Liang, Lu Yin, Kexin Liu, Ying He, Mingming Chen, Haijuan Tang, Sunlu Chen, Sergey Shabala, Hongsheng Zhang and Jinping Cheng
J Integr Plant Biol 2024, 66 (4): 731-748.
doi:
10.1111/jipb.13642
Abstract
(Browse
147
) |
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Soil salinity has a major impact on rice seed germination, severely limiting rice production. Herein, a rice
germination defective
mutant under
salt stress
(
gdss
) was identified by using chemical mutagenesis. The
GDSS
gene was detected via MutMap and shown to encode potassium transporter OsHAK9. Phenotypic analysis of complementation and mutant lines demonstrated that
OsHAK9
was an essential regulator responsible for seed germination under salt stress.
OsHAK9
is highly expressed in germinating seed embryos. Ion contents and non-invasive micro-test technology results showed that OsHAK9 restricted K
+
efflux in salt-exposed germinating seeds for the balance of K
+
/Na
+
. Disruption of
OsHAK9
significantly reduced gibberellin 4 (GA
4
) levels, and the germination defective phenotype of
oshak9a
was partly rescued by exogenous GA
3
treatment under salt stress. RNA sequencing (RNA-seq) and real-time quantitative polymerase chain reaction analysis demonstrated that the disruption of
OsHAK9
improved the GA-deactivated gene
OsGA2ox7
expression in germinating seeds under salt stress, and the expression of
OsGA2ox7
was significantly inhibited by salt stress. Null mutants of
OsGA2ox7
created using clustered, regularly interspaced, short palindromic repeat (CRISPR)/CRISPR-associated nuclease 9 approach displayed a dramatically increased seed germination ability under salt stress. Overall, our results highlight that
OsHAK9
regulates seed germination performance under salt stress involving preventing GA degradation by mediating
OsGA2ox7
, which provides a novel clue about the relationship between GA and
OsHAKs
in rice.
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Designing salt stress-resilient crops: Current progress and future challenges
Xiaoyan Liang, Jianfang Li, Yongqing Yang, Caifu Jiang and Yan Guo
J Integr Plant Biol 2024, 66 (3): 303-329.
doi:
10.1111/jipb.13599
Abstract
(Browse
253
) |
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Excess soil salinity affects large regions of land and is a major hindrance to crop production worldwide. Therefore, understanding the molecular mechanisms of plant salt tolerance has scientific importance and practical significance. In recent decades, studies have characterized hundreds of genes associated with plant responses to salt stress in different plant species. These studies have substantially advanced our molecular and genetic understanding of salt tolerance in plants and have introduced an era of molecular design breeding of salt-tolerant crops. This review summarizes our current knowledge of plant salt tolerance, emphasizing advances in elucidating the molecular mechanisms of osmotic stress tolerance, salt-ion transport and compartmentalization, oxidative stress tolerance, alkaline stress tolerance, and the trade-off between growth and salt tolerance. We also examine recent advances in understanding natural variation in the salt tolerance of crops and discuss possible strategies and challenges for designing salt stress-resilient crops. We focus on the model plant Arabidopsis (
Arabidopsis thaliana
) and the four most-studied crops: rice (
Oryza sativa
), wheat (
Triticum aestivum
), maize (
Zea mays
), and soybean (
Glycine max
).
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Reactive oxygen species: Multidimensional regulators of plant adaptation to abiotic stress and development
Pengtao Wang, Wen‐Cheng Liu, Chao Han, Situ Wang, Ming‐Yi Bai and Chun‐Peng Song
J Integr Plant Biol 2024, 66 (3): 330-367.
doi:
10.1111/jipb.13601
Abstract
(Browse
294
) |
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Reactive oxygen species (ROS) are produced as undesirable by-products of metabolism in various cellular compartments, especially in response to unfavorable environmental conditions, throughout the life cycle of plants. Stress-induced ROS production disrupts normal cellular function and leads to oxidative damage. To cope with excessive ROS, plants are equipped with a sophisticated antioxidative defense system consisting of enzymatic and non-enzymatic components that scavenge ROS or inhibit their harmful effects on biomolecules. Nonetheless, when maintained at relatively low levels, ROS act as signaling molecules that regulate plant growth, development, and adaptation to adverse conditions. Here, we provide an overview of current approaches for detecting ROS. We also discuss recent advances in understanding ROS signaling, ROS metabolism, and the roles of ROS in plant growth and responses to various abiotic stresses.
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Integrative regulatory mechanisms of stomatal movements under changing climate
Jingbo Zhang, Xuexue Chen, Yajing Song and Zhizhong Gong
J Integr Plant Biol 2024, 66 (3): 368-393.
doi:
10.1111/jipb.13611
Abstract
(Browse
158
) |
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Global climate change-caused drought stress, high temperatures and other extreme weather profoundly impact plant growth and development, restricting sustainable crop production. To cope with various environmental stimuli, plants can optimize the opening and closing of stomata to balance CO
2
uptake for photosynthesis and water loss from leaves. Guard cells perceive and integrate various signals to adjust stomatal pores through turgor pressure regulation. Molecular mechanisms and signaling networks underlying the stomatal movements in response to environmental stresses have been extensively studied and elucidated. This review focuses on the molecular mechanisms of stomatal movements mediated by abscisic acid, light, CO
2
, reactive oxygen species, pathogens, temperature, and other phytohormones. We discussed the significance of elucidating the integrative mechanisms that regulate stomatal movements in helping design smart crops with enhanced water use efficiency and resilience in a climate-changing world.
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How plants sense and respond to osmotic stress
Bo Yu, Dai‐Yin Chao and Yang Zhao
J Integr Plant Biol 2024, 66 (3): 394-423.
doi:
10.1111/jipb.13622
Abstract
(Browse
144
) |
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Drought is one of the most serious abiotic stresses to land plants. Plants sense and respond to drought stress to survive under water deficiency. Scientists have studied how plants sense drought stress, or osmotic stress caused by drought, ever since Charles Darwin, and gradually obtained clues about osmotic stress sensing and signaling in plants. Osmotic stress is a physical stimulus that triggers many physiological changes at the cellular level, including changes in turgor, cell wall stiffness and integrity, membrane tension, and cell fluid volume, and plants may sense some of these stimuli and trigger downstream responses. In this review, we emphasized water potential and movements in organisms, compared putative signal inputs in cell wall-containing and cell wall-free organisms, prospected how plants sense changes in turgor, membrane tension, and cell fluid volume under osmotic stress according to advances in plants, animals, yeasts, and bacteria, summarized multilevel biochemical and physiological signal outputs, such as plasma membrane nanodomain formation, membrane water permeability, root hydrotropism, root halotropism, Casparian strip and suberin lamellae, and finally proposed a hypothesis that osmotic stress responses are likely to be a cocktail of signaling mediated by multiple osmosensors. We also discussed the core scientific questions, provided perspective about the future directions in this field, and highlighted the importance of robust and smart root systems and efficient source-sink allocations for generating future high-yield stress-resistant crops and plants.
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IbNIEL-mediated degradation of IbNAC087 regulates jasmonic acid-dependent salt and drought tolerance in sweet potato
Xu Li, Zhen Wang, Sifan Sun, Zhuoru Dai, Jun Zhang, Wenbin Wang, Kui Peng, Wenhao Geng, Shuanghong Xia, Qingchang Liu, Hong Zhai, Shaopei Gao, Ning Zhao, Feng Tian, Huan Zhang and Shaozhen He
J Integr Plant Biol 2024, 66 (2): 176-195.
doi:
10.1111/jipb.13612
Abstract
(Browse
100
) |
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Sweet potato (
Ipomoea batatas
[L.] Lam.) is a crucial staple and bioenergy crop. Its abiotic stress tolerance holds significant importance in fully utilizing marginal lands. Transcriptional processes regulate abiotic stress responses, yet the molecular regulatory mechanisms in sweet potato remain unclear. In this study, a NAC (NAM, ATAF1/2, and CUC2) transcription factor,
IbNAC087
, was identified, which is commonly upregulated in salt- and drought-tolerant germplasms. Overexpression of
IbNAC087
increased salt and drought tolerance by increasing jasmonic acid (JA) accumulation and activating reactive oxygen species (ROS) scavenging, whereas silencing this gene resulted in opposite phenotypes. JA-rich
IbNAC087
-OE (overexpression) plants exhibited more stomatal closure than wild-type (WT) and
IbNAC087
-Ri plants under NaCl, polyethylene glycol, and methyl jasmonate treatments. IbNAC087 functions as a nuclear transcriptional activator and directly activates the expression of the key JA biosynthesis-related genes
lipoxygenase
(
IbLOX
) and
allene oxide synthase
(
IbAOS
). Moreover, IbNAC087 physically interacted with a RING-type E3 ubiquitin ligase NAC087-INTERACTING E3 LIGASE (IbNIEL), negatively regulating salt and drought tolerance in sweet potato. IbNIEL ubiquitinated IbNAC087 to promote 26S proteasome degradation, which weakened its activation on
IbLOX
and
IbAOS
. The findings provide insights into the mechanism underlying the IbNIEL-IbNAC087 module regulation of JA-dependent salt and drought response in sweet potato and provide candidate genes for improving abiotic stress tolerance in crops.
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Heat Shock Factor A1s are required for phytochrome-interacting factor 4-mediated thermomorphogenesis in Arabidopsis
Bingjie Li, Shimeng Jiang, Liang Gao, Wenhui Wang, Haozheng Luo, Yining Dong, Zhihua Gao, Shuzhi Zheng, Xinye Liu and Wenqiang Tang
J Integr Plant Biol 2024, 66 (1): 20-35.
DOI:
10.1111/jipb.13579
Abstract
(Browse
187
) |
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Thermomorphogenesis and the heat shock (HS) response are distinct thermal responses in plants that are regulated by PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) and HEAT SHOCK FACTOR A1s (HSFA1s), respectively. Little is known about whether these responses are interconnected and whether they are activated by similar mechanisms. An analysis of transcriptome dynamics in response to warm temperature (28℃) treatment revealed that 30 min of exposure activated the expression of a subset of HSFA1 target genes in
Arabidopsis thaliana
. Meanwhile, a loss-of-function
HSFA1
quadruple mutant (
hsfa1-cq
) was insensitive to warm temperature-induced hypocotyl growth. In
hsfa1-cq
plants grown at 28℃, the protein and transcript levels of PIF4 were greatly reduced, and the circadian rhythm of many thermomorphogenesis-related genes (including
PIF4
) was disturbed. Additionally, the nuclear localization of HSFA1s and the binding of HSFA1d to the
PIF4
promoter increased following warm temperature exposure, whereas
PIF4
overexpression in
hsfa1-cq
partially rescued the altered warm temperature-induced hypocotyl growth of the mutant. Taken together, these results suggest that HSFA1s are required for PIF4 accumulation at a warm temperature, and they establish a central role for HSFA1s in regulating both thermomorphogenesis and HS responses in Arabidopsis.
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TaSRO1 interacts with TaVP1 to modulate seed dormancy and pre-harvest sprouting resistance in wheat
Shupeng Liu, Li Li, Wenlong Wang, Guangmin Xia and Shuwei Liu
J Integr Plant Biol 2024, 66 (1): 36-53.
DOI:
10.1111/jipb.13600
Abstract
(Browse
119
) |
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Dormancy is an adaptive trait which prevents seeds from germinating under unfavorable environmental conditions. Seeds with weak dormancy undergo pre-harvest sprouting (PHS) which decreases grain yield and quality. Understanding the genetic mechanisms that regulate seed dormancy and resistance to PHS is crucial for ensuring global food security. In this study, we illustrated the function and molecular mechanism of TaSRO1 in the regulation of seed dormancy and PHS resistance by suppressing TaVP1. The
tasro1
mutants exhibited strong seed dormancy and enhanced resistance to PHS, whereas the mutants of
tavp1
displayed weak dormancy. Genetic evidence has shown that
TaVP1
is epistatic to
TaSRO1
. Biochemical evidence has shown that TaSRO1 interacts with TaVP1 and represses the transcriptional activation of the PHS resistance genes
TaPHS1
and
TaSdr
. Furthermore, TaSRO1 undermines the synergistic activation of TaVP1 and TaABI5 in PHS resistance genes. Finally, we highlight the great potential of
tasro1
alleles for breeding elite wheat cultivars that are resistant to PHS.
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NFXL1 functions as a transcriptional activator required for thermotolerance at reproductive stage in Arabidopsis
Qiao‐Yun Zhu, Lin‐Lin Zhang and Jian‐Xiang Liu
J Integr Plant Biol 2024, 66 (1): 54-65.
DOI:
10.1111/jipb.13604
Abstract
(Browse
145
) |
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Plants are highly susceptible to abiotic stresses, particularly heat stress during the reproductive stage. However, the specific molecular mechanisms underlying this sensitivity remain largely unknown. In the current study, we demonstrate that the Nuclear Transcription Factor, X-box Binding Protein 1-Like 1 (NFXL1), directly regulates the expression of
DEHYDRATION-RESPONSIVE ELEMENT-BINDING PROTEIN
2A (DREB2A), which is crucial for reproductive thermotolerance in Arabidopsis.
NFXL1
is upregulated by heat stress, and its mutation leads to a reduction in silique length (seed number) under heat stress conditions. RNA-Seq analysis reveals that NFXL1 has a global impact on the expression of heat stress responsive genes, including
DREB2A
,
Heat Shock Factor A3
(
HSFA3
) and
Heat Shock Protein 17.6
(
HSP17.6
) in flower buds. Interestingly, NFXL1 is enriched in the promoter region of
DREB2A
, but not of either
HSFA3
or
HSP17.6
. Further experiments using electrophoretic mobility shift assay have confirmed that NFXL1 directly binds to the DNA fragment derived from the
DREB2A
promoter. Moreover, effector–reporter assays have shown that NFXL1 activates the
DREB2A
promoter. The
DREB2A
mutants are also heat stress sensitive at the reproductive stage, and
DEREB2A
is epistatic to
NFXL1
in regulating thermotolerance in flower buds. It is known that
HSFA3
, a direct target of DREB2A, regulates the expression of heat shock proteins genes under heat stress conditions. Thus, our findings establish NFXL1 as a critical upstream regulator of
DREB2A
in the transcriptional cassette responsible for heat stress responses required for reproductive thermotolerance in Arabidopsis.
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The m
6
A reader SiYTH1 enhances drought tolerance by affecting the messenger RNA stability of genes related to stomatal closure and reactive oxygen species scavenging in
Setaria italica
Weiwei Luo, Yuxiang Tang, Shenglan Li, Linlin Zhang, Yuwei Liu, Renliang Zhang, Xianmin Diao and Jingjuan Yu
J Integr Plant Biol 2023, 65 (12): 2569-2586.
DOI:
10.1111/jipb.13575
Abstract
(Browse
171
) |
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Foxtail millet (
Setaria italica
), a vital drought-resistant crop, plays a significant role in ensuring food and nutritional security. However, its drought resistance mechanism is not fully understood.
N
6
-methyladenosine (m
6
A) modification of RNA, a prevalent epi-transcriptomic modification in eukaryotes, provides a binding site for m
6
A readers and affects plant growth and stress responses by regulating RNA metabolism. In this study, we unveiled that the
YT521-B homology
(
YTH
) family gene
SiYTH1
positively regulated the drought tolerance of foxtail millet. Notably, the
siyth1
mutant exhibited reduced stomatal closure and augmented accumulation of excessive H
2
O
2
under drought stress. Further investigations demonstrated that SiYTH1 positively regulated the transcripts harboring m
6
A modification related to stomatal closure and reactive oxygen species (ROS) scavenging under drought stress. SiYTH1 was uniformly distributed in the cytoplasm of
SiYTH1-GFP
transgenic foxtail millet. It formed dynamic liquid-like SiYTH1 cytosol condensates in response to drought stress. Moreover, the cytoplasmic protein SiYTH1 was identified as a distinct m
6
A reader, facilitating the stabilization of its directly bound
SiARDP
and ROS scavenging-related transcripts under drought stress. Furthermore, natural variation analysis revealed
SiYTH1
AGTG
as the dominant allele responsible for drought tolerance in foxtail millet. Collectively, this study provides novel insights into the intricate mechanism of m
6
A reader-mediated drought tolerance and presents a valuable genetic resource for improving drought tolerance in foxtail millet breeding.
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The SlWRKY57-SlVQ21/SlVQ16 module regulates salt stress in tomato
Jilin Ma, Chonghua Li, Lulu Sun, Xuechun Ma, Hui Qiao, Wenchao Zhao, Rui Yang, Susheng Song, Shaohui Wang and Huang Huang
J Integr Plant Biol 2023, 65 (11): 2437-2455.
DOI:
10.1111/jipb.13562
Abstract
(Browse
314
) |
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Salt stress is a major abiotic stress which severely hinders crop production. However, the regulatory network controlling tomato resistance to salt remains unclear. Here, we found that the tomato WRKY transcription factor WRKY57 acted as a negative regulator in salt stress response by directly attenuating the transcription of salt-responsive genes (
SlRD29B
and
SlDREB2
) and an ion homeostasis gene (
SlSOS1
). We further identified two VQ-motif containing proteins SlVQ16 and SlVQ21 as SlWRKY57-interacting proteins. SlVQ16 positively, while SlVQ21 negatively modulated tomato resistance to salt stress. SlVQ16 and SlVQ21 competitively interacted with SlWRKY57 and antagonistically regulated the transcriptional repression activity of SlWRKY57. Additionally, the SlWRKY57-SlVQ21/SlVQ16 module was involved in the pathway of phytohormone jasmonates (JAs) by interacting with JA repressors JA-ZIM domain (JAZ) proteins. These results provide new insights into how the SlWRKY57-SlVQ21/SlVQ16 module finely tunes tomato salt tolerance.
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The transcription factor NAC102 confers cadmium tolerance by regulating
WAKL11
expression and cell wall pectin metabolism in
Arabidopsis
Guang Hao Han, Ru Nan Huang, Li Hong Hong, Jia Xi Xu, Yi Guo Hong, Yu Huan Wu and Wei Wei Chen
J Integr Plant Biol 2023, 65 (10): 2262-2278.
DOI:
10.1111/jipb.13557
Abstract
(Browse
279
) |
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Cadmium (Cd) toxicity severely limits plant growth and development. Moreover, Cd accumulation in vegetables, fruits, and food crops poses health risks to animals and humans. Although the root cell wall has been implicated in Cd stress in plants, whether Cd binding by cell wall polysaccharides contributes to tolerance remains controversial, and the mechanism underlying transcriptional regulation of cell wall polysaccharide biosynthesis in response to Cd stress is unknown. Here, we functionally characterized an
Arabidopsis thaliana
NAC-type transcription factor, NAC102, revealing its role in Cd stress responses. Cd stress rapidly induced accumulation of
NAC102.1
, the major transcript encoding functional NAC102, especially in the root apex. Compared to wild type (WT) plants, a
nac102
mutant exhibited enhanced Cd sensitivity, whereas
NAC102.1
-overexpressing plants displayed the opposite phenotype. Furthermore, NAC102 localizes to the nucleus, binds directly to the promoter of
WALL-ASSOCIATED KINASE-LIKE PROTEIN11
(
WAKL11
), and induces transcription, thereby facilitating pectin degradation and decreasing Cd binding by pectin. Moreover,
WAKL11
overexpression restored Cd tolerance in
nac102
mutants to the WT levels, which was correlated with a lower pectin content and lower levels of pectin-bound Cd. Taken together, our work shows that the NAC102-WAKL11 module regulates cell wall pectin metabolism and Cd binding, thus conferring Cd tolerance in
Arabidopsis
.
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TaTIP41 and TaTAP46 positively regulate drought tolerance in wheat by inhibiting PP2A activity
Jianhui Ma, Yuke Geng, Hong Liu, Mengqi Zhang, Shujuan Liu, Chenyang Hao, Jian Hou, Youfu Zhang, Daijing Zhang, Weijun Zhang, Xueyong Zhang and Tian Li
J Integr Plant Biol 2023, 65 (9): 2056-2070.
DOI:
10.1111/jipb.13542
Abstract
(Browse
492
) |
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Drought is a major environmental stress limiting global wheat (
Triticum aestivum
) production. Exploring drought tolerance genes is important for improving drought adaptation in this crop. Here, we cloned and characterized
TaTIP41
, a novel drought tolerance gene in wheat. TaTIP41 is a putative conserved component of target of rapamycin (TOR) signaling, and the
TaTIP41
homoeologs were expressed in response to drought stress and abscisic acid (ABA). The overexpression of
TaTIP41
enhanced drought tolerance and the ABA response, including ABA-induced stomatal closure, while its downregulation using RNA interference (RNAi) had the opposite effect. Furthermore, TaTIP41 physically interacted with TaTAP46, another conserved component of TOR signaling. Like TaTIP41, TaTAP46 positively regulated drought tolerance. Furthermore, TaTIP41 and TaTAP46 interacted with type-2A protein phosphatase (PP2A) catalytic subunits, such as TaPP2A-2, and inhibited their enzymatic activities. Silencing
TaPP2A-2
improved drought tolerance in wheat. Together, our findings provide new insights into the roles of TaTIP41 and TaTAP46 in the drought tolerance and ABA response in wheat, and their potential application in improving wheat environmental adaptability.
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The basic helix-loop-helix transcription factor gene,
OsbHLH38
, plays a key role in controlling rice salt tolerance
Fengping Du, Yinxiao Wang, Juan Wang, Yingbo Li, Yue Zhang, Xiuqin Zhao, Jianlong Xu, Zhikang Li, Tianyong Zhao, Wensheng Wang and Binying Fu
J Integr Plant Biol 2023, 65 (8): 1859-1873.
doi:
10.1111/jipb.13489
Abstract
(Browse
517
) |
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The plant hormone abscisic acid (ABA) is crucial for plant seed germination and abiotic stress tolerance. However, the association between ABA sensitivity and plant abiotic stress tolerance remains largely unknown. In this study, 436 rice accessions were assessed for their sensitivity to ABA during seed germination. The considerable diversity in ABA sensitivity among rice germplasm accessions was primarily reflected by the differentiation between the
Xian
(
indica
) and
Geng
(
japonica
) subspecies and between the upland-
Geng
and lowland-
Geng
ecotypes. The upland-
Geng
accessions were most sensitive to ABA. Genome-wide association analyses identified four major quantitative trait loci containing 21 candidate genes associated with ABA sensitivity of which a basic helix-loop-helix transcription factor gene,
OsbHLH38
, was the most important for ABA sensitivity. Comprehensive functional analyses using knockout and overexpression transgenic lines revealed that
OsbHLH38
expression was responsive to multiple abiotic stresses. Overexpression of
OsbHLH38
increased seedling salt tolerance, while knockout of
OsbHLH38
increased sensitivity to salt stress. A salt-responsive transcription factor,
OsDREB2A
, interacted with OsbHLH38 and was directly regulated by OsbHLH38. Moreover,
OsbHLH38
affected rice abiotic stress tolerance by mediating the expression of a large set of transporter genes of phytohormones, transcription factor genes, and many downstream genes with diverse functions, including photosynthesis, redox homeostasis, and abiotic stress responsiveness. These results demonstrated that
OsbHLH38
is a key regulator in plant abiotic stress tolerance.
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)
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Golgi-localized MORN1 promotes lipid droplet abundance and enhances tolerance to multiple stresses in
Arabidopsis
Zhan Li, Yue Gao, Jiapei Yan, Shuai Wang, Shu Wang, Yuanyuan Liu, Shaokui Wang and Jian Hua
J Integr Plant Biol 2023, 65 (8): 1890-1903.
DOI:
10.1111/jipb.13498
Abstract
(Browse
189
) |
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Lipid droplet (LD) in vegetative tissues has recently been implicated in environmental responses in plants, but its regulation and its function in stress tolerance are not well understood. Here, we identified a
Membrane Occupation and Recognition Nexus 1
(
MORN1
) gene as a contributor to natural variations of stress tolerance through genome-wide association study in
Arabidopsis thaliana
. Characterization of its loss-of-function mutant and natural variants revealed that the
MORN1
gene is a positive regulator of plant growth, disease resistance, cold tolerance, and heat tolerance. The MORN1 protein is associated with the Golgi and is also partly associated with LD. Protein truncations that disrupt these associations abolished the biological function of the MORN1 protein. Furthermore, the
MORN1
gene is a positive regulator of LD abundance, and its role in LD number regulation and stress tolerance is highly linked. Therefore, this study identifies MORN1 as a positive regulator of LD abundance and a contributor to natural variations of stress tolerance. It implicates a potential involvement of Golgi in LD biogenesis and strongly suggests a contribution of LD to diverse processes of plant growth and stress responses.
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NIGT1 represses plant growth and mitigates phosphate starvation signaling to balance the growth response tradeoff in rice
Yuxin Zhang, Qianqian Zhang, Meina Guo, Xueqing Wang, Tianjie Li, Qingyu Wu, Lihui Li, Keke Yi and Wenyuan Ruan
J Integr Plant Biol 2023, 65 (8): 1874-1889.
doi:
10.1111/jipb.13496
Abstract
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Inorganic phosphate (Pi) availability is an important factor which affects the growth and yield of crops, thus an appropriate and effective response to Pi fluctuation is critical. However, how crops orchestrate Pi signaling and growth under Pi starvation conditions to optimize the growth defense tradeoff remains unclear. Here we show that a Pi starvation-induced transcription factor NIGT1 (NITRATE-INDUCIBLE GARP-TYPE TRANSCRIPTIONAL REPRESSOR 1) controls plant growth and prevents a hyper-response to Pi starvation by directly repressing the expression of growth-related and Pi-signaling genes to achieve a balance between growth and response under a varying Pi environment. NIGT1 directly binds to the promoters of Pi starvation signaling marker genes, like
IPS1
,
miR827
, and
SPX2
, under Pi-deficient conditions to mitigate the Pi-starvation responsive (PSR). It also directly represses the expression of vacuolar Pi efflux transporter genes
VPE1/2
to regulate plant Pi homeostasis. We further demonstrate that NIGT1 constrains shoot growth by repressing the expression of growth-related regulatory genes, including brassinolide signal transduction master regulator
BZR1
, cell division regulator
CYCB1;1
, and DNA replication regulator
PSF3
. Our findings reveal the function of NIGT1 in orchestrating plant growth and Pi starvation signaling, and also provide evidence that NIGT1 acts as a safeguard to avoid hyper-response during Pi starvation stress in rice.
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The salt-activated CBF1/CBF2/CBF3-GALS1 module fine-tunes galactan-induced salt hypersensitivity in
Arabidopsis
Jingwei Yan, Ya Liu, Jiawen Yan, Zhihui Liu, Heqiang Lou and Jiasheng Wu
J Integr Plant Biol 2023, 65 (8): 1904-1917.
DOI:
10.1111/jipb.13501
Abstract
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236
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Plant growth and development are significantly hampered in saline environments, limiting agricultural productivity. Thus, it is crucial to unravel the mechanism underlying plant responses to salt stress. β-1,4-Galactan (galactan), which forms the side chains of pectic rhamnogalacturonan I, enhances plant sensitivity to high-salt stress. Galactan is synthesized by GALACTAN SYNTHASE1 (GALS1). We previously showed that NaCl relieves the direct suppression of
GALS1
transcription by the transcription factors BPC1 and BPC2 to induce the excess accumulation of galactan in
Arabidopsis
(
Arabidopsis thaliana
). However, how plants adapt to this unfavorable environment remains unclear. Here, we determined that the transcription factors CBF1, CBF2, and CBF3 directly interact with the
GALS1
promoter and repress its expression, leading to reduced galactan accumulation and enhanced salt tolerance. Salt stress enhances the binding of CBF1/CBF2/CBF3 to the
GALS1
promoter by inducing CBF1/CBF2/CBF3 transcription and accumulation. Genetic analysis suggested that CBF1/CBF2/CBF3 function upstream of GALS1 to modulate salt-induced galactan biosynthesis and the salt response. CBF1/CBF2/CBF3 and BPC1/BPC2 function in parallel to regulate
GALS1
expression, thereby modulating the salt response. Our results reveal a mechanism in which salt-activated CBF1/CBF2/CBF3 inhibit BPC1/BPC2-regulated
GALS1
expression to alleviate galactan-induced salt hypersensitivity, providing an activation/deactivation fine-tune mechanism for dynamic regulation of
GALS1
expression under salt stress in
Arabidopsis
.
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Zinc-finger protein GmZF351 improves both salt and drought stress tolerance in soybean
Wei Wei, Long Lu, Xiao‐Hua Bian, Qing‐Tian Li, Jia‐Qi Han, Jian‐Jun Tao, Cui‐Cui Yin, Yong‐Cai Lai, Wei Li, Ying‐Dong Bi, Wei‐Qun Man, Shou‐Yi Chen, Jin‐Song Zhang and Wan‐Ke Zhang
J Integr Plant Biol 2023, 65 (7): 1636-1650.
doi:
10.1111/jipb.13474
Abstract
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264
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Abiotic stress is one of the most important factors reducing soybean yield. It is essential to identify regulatory factors contributing to stress responses. A previous study found that the tandem CCCH zinc-finger protein GmZF351 is an oil level regulator. In this study, we discovered that the
GmZF351
gene is induced by stress and that the overexpression of
GmZF351
confers stress tolerance to transgenic soybean. GmZF351 directly regulates the expression of
GmCIPK9
and
GmSnRK
, leading to stomata closing, by binding to their promoter regions, which carry two CT(G/C)(T/A)AA elements. Stress induction of
GmZF351
is mediated through reduction in the H3K27me3 level at the
GmZF351
locus. Two
JMJ30-demethylase-like
genes,
GmJMJ30-1
and
GmJMJ30-2
, are involved in this demethylation process. Overexpression of
GmJMJ30-1/2
in transgenic hairy roots enhances
GmZF351
expression mediated by histone demethylation and confers stress tolerance to soybean. Yield-related agronomic traits were evaluated in stable
GmZF351
-transgenic plants under mild drought stress conditions. Our study reveals a new mode of GmJMJ30-GmZF351 action in stress tolerance, in addition to that of GmZF351 in oil accumulation. Manipulation of the components in this pathway is expected to improve soybean traits and adaptation under unfavorable environments.
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OsWR2 recruits HDA704 to regulate the deacetylation of H4K8ac in the promoter of
OsABI5
in response to drought stress
Yalu Guo, Yiqing Tan, Minghao Qu, Kai Hong, Longjun Zeng, Lei Wang, Chuxiong Zhuang, Qian Qian, Jiang Hu and Guosheng Xiong
J Integr Plant Biol 2023, 65 (7): 1651-1669.
DOI:
10.1111/jipb.13481
Abstract
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Drought stress is a major environmental factor that limits the growth, development, and yield of rice (
Oryza sativa
L.). Histone deacetylases (HDACs) are involved in the regulation of drought stress responses. HDA704 is an RPD3/HDA1 class HDAC that mediates the deacetylation of H4K8 (lysine 8 of histone H4) for drought tolerance in rice. In this study, we show that plants overexpressing
HDA704
(
HDA704
-OE) are resistant to drought stress and sensitive to abscisic acid (ABA), whereas
HDA704
knockout mutant (
hda704
) plants displayed decreased drought tolerance and ABA sensitivity. Transcriptome analysis revealed that HDA704 regulates the expression of ABA-related genes in response to drought stress. Moreover, HDA704 was recruited by a drought-resistant transcription factor, WAX SYNTHESIS REGULATORY 2 (OsWR2), and co-regulated the expression of the ABA biosynthesis genes
NINE-CIS-EPOXYCAROTENOID DIOXYGENASE 3
(
NCED3
),
NCED4
, and
NCED5
under drought stress. HDA704 also repressed the expression of
ABA-INSENSITIVE 5
(
OsABI5
) and
DWARF AND SMALL SEED 1
(
OsDSS1
) by regulating H4K8ac levels in the promoter regions in response to polyethylene glycol 6000 treatment. In agreement, the loss of OsABI5 function increased resistance to dehydration stress in rice. Our results demonstrate that HDA704 is a positive regulator of the drought stress response and offers avenues for improving drought resistance in rice.
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The endo-beta mannase MAN7 contributes to cadmium tolerance by modulating root cell wall binding capacity in
Arabidopsis thaliana
Qi Wu, Yu Ting Meng, Zhi Hang Feng, Ren Fang Shen and Xiao Fang Zhu
J Integr Plant Biol 2023, 65 (7): 1670-1686.
DOI:
10.1111/jipb.13487
Abstract
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The heavy metal cadmium (Cd) is detrimental to crop growth and threatens human health through the food chain. To cope with Cd toxicity, plants employ multiple strategies to decrease Cd uptake and its root-to-shoot translocation. However, genes that participate in the Cd-induced transcriptional regulatory network, including those encoding transcription factors, remain largely unidentified. In this study, we demonstrate that ENDO-BETA-MANNASE 7 (MAN7) is necessary for the response of
Arabidopsis thaliana
to toxic Cd levels. We show that MAN7 is responsible for mannase activity and modulates mannose content in the cell wall, which plays a role in Cd compartmentalization in the cell wall under Cd toxicity conditions. Additionally, the repression of root growth by Cd was partially reversed via exogenous application of mannose, suggesting that MAN7-mediated cell wall Cd redistribution depends on the mannose pathway. Notably, we identified a basic leucine zipper (bZIP) transcription factor, bZIP44, that acts upstream of MAN7 in response to Cd toxicity. Transient dual-luciferase assays indicated that bZIP44 directly binds to the
MAN7
promoter region and activates its transcription. Loss of bZIP44 function was associated with greater sensitivity to Cd treatment and higher accumulation of the heavy metal in roots and shoots. Moreover,
MAN7
overexpression relieved the inhibition of root elongation seen in the
bzip44
mutant under Cd toxicity conditions. This study thus reveals a pathway showing that
MAN7
-associated Cd tolerance in
Arabidopsis
is controlled by bZIP44 upon Cd exposure.
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The Sm core protein SmEb regulates salt stress responses through maintaining proper splicing of
RCD1
pre-mRNA in
Arabidopsis
Yechun Hong, Yang Gao, Jia Pang, Huazhong Shi, Tingting Li, Huiying Meng, Dali Kong, Yunjuan Chen, Jian-Kang Zhu and Zhen Wang
J Integr Plant Biol 2023, 65 (6): 1383-1393.
DOI:
10.1111/jipb.13457
Abstract
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Salt stress adversely impacts crop production. Several spliceosome components have been implicated in regulating salt stress responses in plants, however, the underlying molecular basis is still unclear. Here we report that the spliceosomal core protein SmEb is essential to salt tolerance in Arabidopsis. Transcriptome analysis showed that SmEb modulates alternative splicing of hundreds of pre-mRNAs in plant response to salt stress. Further study revealed that SmEb is crucial in maintaining proper ratio of two
RCD1
splicing variants (
RCD1.1/ RCD1.2
) important for salt stress response. In addition, RCD1.1 but not RCD1.2 is able to interact with the stress regulators and attenuates salt- sensitivity by decreasing salt-induced cell death in
smeb-1
mutant. Together, our findings uncovered the essential role of SmEb in the regulation of alternative pre-mRNA splicing in salt stress response.
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The alleviation of ammonium toxicity in plants
Chengbin Xiao, Yuan Fang, Suomin Wang and Kai He
J Integr Plant Biol 2023, 65 (6): 1362-1368.
doi:
10.1111/jipb.13467
Abstract
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Nitrogen (N) is an essential macronutrient for plants and profoundly affects crop yields and qualities. Ammonium (NH
4
+
) and nitrate (NO
3
?
) are major inorganic N forms absorbed by plants from the surrounding environments. Intriguingly, NH
4
+
is usually toxic to plants when it serves as the sole or dominant N source. It is thus important for plants to coordinate the utilization of NH
4
+
and the alleviation of NH
4
+
toxicity. To fully decipher the molecular mechanisms underlying how plants minimize NH
4
+
toxicity may broadly benefit agricultural practice. In the current minireview, we attempt to discuss recent discoveries in the strategies for mitigating NH
4
+
toxicity in plants, which may provide potential solutions for improving the nitrogen use efficiency (NUE) and stress adaptions in crops.
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The spliceophilin CYP18‐2 is mainly involved in the splicing of retained introns under heat stress in
Arabidopsis
Areum Lee, Hyun Ji Park, Seung Hee Jo, Haemyeong Jung, Hyun‐Soon Kim, Hyo‐Jun Lee, Youn‐Sung Kim, Choonkyun Jung and Hye Sun Cho
J Integr Plant Biol 2023, 65 (5): 1113-1133.
doi:
10.1111/jipb.13450
Abstract
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Peptidyl‐prolyl isomerase‐like 1 (PPIL1) is associated with the human spliceosome complex. However, its function in pre‐mRNA splicing remains unclear. In this study, we show that
Arabidopsis thaliana
CYCLOPHILIN 18‐2 (AtCYP18‐2), a PPIL1 homolog, plays an essential role in heat tolerance by regulating pre‐mRNA splicing. Under heat stress conditions,
AtCYP18‐2
expression was upregulated in mature plants and GFP‐tagged AtCYP18‐2 redistributed to nuclear and cytoplasmic puncta. We determined that AtCYP18‐2 interacts with several spliceosome complex B
ACT
components in nuclear puncta and is primarily associated with the small nuclear RNAs
U5
and
U6
in response to heat stress. The
AtCYP18‐2
loss‐of‐function allele
cyp18‐2
engineered by CRISPR/Cas9‐mediated gene editing exhibited a hypersensitive phenotype to heat stress relative to the wild type. Moreover, global transcriptome profiling showed that the
cyp18‐2
mutation affects alternative splicing of heat stress–responsive genes under heat stress conditions, particularly intron retention (IR). The abundance of most intron‐containing transcripts of a subset of genes essential for thermotolerance decreased in
cyp18‐2
compared to the wild type. Furthermore, the intron‐containing transcripts of two heat stress‐related genes,
HEAT SHOCK PROTEIN 101 (HSP101)
and
HEAT SHOCK FACTOR A2
(
HSFA2
), produced functional proteins. HSP101‐IR‐GFP localization was responsive to heat stress, and HSFA2‐III‐IR interacted with HSF1 and HSP90.1 in plant cells. Our findings reveal that CYP18‐2 functions as a splicing factor within the B
ACT
spliceosome complex and is crucial for ensuring the production of adequate levels of alternatively spliced transcripts to enhance thermotolerance.
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Editorial Office, Journal of Integrative Plant Biology, Institute of Botany, CAS
No. 20 Nanxincun, Xiangshan, Beijing 100093, China
Tel: +86 10 6283 6133 Fax: +86 10 8259 2636 E-mail: jipb@ibcas.ac.cn
Copyright © 2022 by the Institute of Botany, the Chinese Academy of Sciences
Online ISSN: 1744-7909 Print ISSN: 1672-9072 CN: 11-5067/Q
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