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Review

Function of Chloroplasts in Plant Stress Responses

by
Yun Song
1,†,
Li Feng
2,3,†,
Mohammed Abdul Muhsen Alyafei
4,
Abdul Jaleel
4 and
Maozhi Ren
2,3,*
1
School of Life Sciences, Liaocheng University, Liaocheng 252000, China
2
Institute of Urban Agriculture, Chinese Academy of Agricultural Sciences, Chengdu 610213, China
3
Zhengzhou Research Base, State Key Laboratory of Cotton Biology, Zhengzhou University, Zhengzhou 450001, China
4
Department of Integrative Agriculture, College of Agriculture and Veterinary Medicine, United Arab Emirates University, Al Ain P.O. Box 15551, United Arab Emirates
*
Author to whom correspondence should be addressed.
†
These authors have contributed equally to this work and share first authorship.
Int. J. Mol. Sci. 2021, 22(24), 13464; https://doi.org/10.3390/ijms222413464
Submission received: 30 October 2021 / Revised: 6 December 2021 / Accepted: 13 December 2021 / Published: 15 December 2021
(This article belongs to the Special Issue Chloroplast and Stress Signaling)
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Abstract

:
The chloroplast has a central position in oxygenic photosynthesis and primary metabolism. In addition to these functions, the chloroplast has recently emerged as a pivotal regulator of plant responses to abiotic and biotic stress conditions. Chloroplasts have their own independent genomes and gene-expression machinery and synthesize phytohormones and a diverse range of secondary metabolites, a significant portion of which contribute the plant response to adverse conditions. Furthermore, chloroplasts communicate with the nucleus through retrograde signaling, for instance, reactive oxygen signaling. All of the above facilitate the chloroplast’s exquisite flexibility in responding to environmental stresses. In this review, we summarize recent findings on the involvement of chloroplasts in plant regulatory responses to various abiotic and biotic stresses including heat, chilling, salinity, drought, high light environmental stress conditions, and pathogen invasions. This review will enrich the better understanding of interactions between chloroplast and environmental stresses, and will lay the foundation for genetically enhancing plant-stress acclimatization.

1. Introduction

As sessile organisms, plants have to cope with various environmental conditions that are unfavorable or stressful for their growth and development. These adverse environmental conditions include abiotic stresses such as drought, heat, chilling/freezing, salinity, and nutrient deficiency as well as biotic stresses such as herbivore attack and pathogen infection [1,2,3,4]. These abiotic and biotic stresses limit crop yields and cause tremendous economic losses. These adverse effects are getting worse due to climate change, increasing population, and less arable land [1,2]. Plants have evolved a number of strategies to sense stress signals and adapt to adverse environments. Increasing evidence has revealed the essential role of the chloroplast, an organelle for photosynthesis in green plants, in plant stress response and stress adaption [3,4,5].
The chloroplast is a double-membrane plant endosymbiotic organelle where photosynthesis takes place [5,6,7,8]. Chloroplasts have retained their own genomes, and the chloroplast genome contains approximately 120 genes involved in chloroplast activities such as energy production and gene expression [9,10]. Chloroplasts produce energy through photosynthesis and oxygen-release processes, which sustain plant growth and crop yield. As such, chloroplasts are responsible for the biosynthesis of active compounds such as amino acids, phytohormones, nucleotides, vitamins, lipids, and secondary metabolites [9]. Furthermore, the chloroplast plays a vital role in plant acclimation to environmental stresses [3,4,6]. When plants are in adverse environmental conditions, chloroplasts sense these stresses and synthesize biologically active compounds and phytohormones, which protect plants from environmental stresses. In addition, chloroplasts communicate with the nucleus through plastid-to-nucleus retrograde signaling to acclimate to environmental stresses (Figure 1) [3,11,12].
Retrograde signaling pathways refer to the communications from the plastid to the nucleus [13]. The chloroplast functions as an environmental sensor. Fluctuations in the environment perturb chloroplast homeostasis, and the disturbance then drives the chloroplasts to communicate with the nucleus through retrograde signals. Eventually, plants remodel metabolism and gene expression to adapt to external stresses [7,11,12,13,14,15]. The retrograde signaling typically includes tetrapyrroles, phosphoadenosines, carotenoid oxidation products, isoprenoid precursors, carbohydrate metabolites, and reactive oxygen species (ROS) [16,17,18,19,20,21,22,23].
Under a series of unfavorable environmental conditions, chloroplasts generate the ROS retrograde signals including superoxide anion (O2−), hydrogen peroxide (H2O2), hydroxyl radical (OH▪), and singlet oxygen (1O2) [7,18,24,25,26,27]. The ROS in plants can severely threaten their health and viability. However, under stressful conditions, ROS function as a retrograde signal and modify the nuclear transcriptome to cope with these adverse stresses. Plants have evolved many strategies to maintain ROS dynamic equilibrium and normal photosynthetic efficiency, including complicated redox reaction chains and the ROS-scavenging system [18,26,27]. Singlet oxygen is generated at photosystem II (PSII) under high-light conditions through the excitation of ground-state triplet oxygen [7,11,24,28,29]. The singlet-oxygen-mediated transcriptional responses were first identified in the flu Arabidopsis mutant [30,31]. The functional FLU protein is a nuclear-encoded plastid protein that negatively regulates chlorophyll biosynthesis and consequently accumulates the strongly photosensitizing chlorophyll precursor protochlorophyllide. When dark-treated flu mutants are moved into the light, the mutants specifically accumulate singlet oxygen [32]. The singlet oxygen regulates a set of nuclear genes called singlet oxygen-responsive genes (SORGs), and most of these genes play a role in photosynthesis, carbon metabolism and plastid mRNA processing [7,33]. The activity of singlet oxygen signaling requires two nuclear-encoded proteins, Executor (Ex) 1 and 2, which are located in the thylakoid membrane of chloroplasts [31,32,34,35,36,37]. Furthermore, it has been reported that the plastid ATP-dependent zinc metalloprotease FtsH2 is involved in EX1/EX2 signaling [38,39]. Studies also find that β-cyclocitral is another singlet oxygen signaling pathway, which occurs independently of EX1 and EX2 [38,39,40]. Hydrogen peroxide acts as another retrograde signaling molecule. The specific role of hydrogen peroxide is identified through an RNAi line of thylakoid membrane-bound ascorbate peroxidase (tAPX) [41]. A number of putative components of the hydrogen peroxide signal transduction network were identified, including a series of transcription factors, mitogenactivated protein kinases (MAPKs) and miRNAs [7,42].
Methylerythritol cyclodiphosphate (MEcPP), an intermediate of the methylerythritol phosphate (MEP) pathway for plastid isoprenoid biosynthesis, functions as another retrograde signal to activate stress-responsive nuclear gene expression [23,43]. MEcPP was first identified by screening for mutants with elicited expression of hydroxyperoxide lyase (HPL). HPL is a nuclear stress-responsive gene and encodes a chloroplast enzyme, which plays a fundamental role in the defense-related molecules (such as the hormone jasmonic acid JA) synthesis [43]. The constitutively expressing HPL (ceh1) mutant was discovered. When exposed to high light or wounding stresses, plants accumulate MEcPP and regulate the expression of a series of nuclear genes [23,43,44,45]. Phosphonucleotide 3′-phosphoadenosine 5′-phosphate (PAP) is an important plastid metabolite and recently has emerged as a new retrograde signal for plant stress responses [16,46,47]. Chloroplast 3′ (2′), 5′-bisphosphate nucleotidase SAL1 can dephosphorylate PAP to adenosine monophosphate (AMP). When plants respond to drought and high light stresses, the activity of SAL1 is inhibited and PAP thus accumulates. PAP can regulate a series of nuclear stress-responsive genes [7]. Recent research has revealed the role of PAP in the drought stress response through regulating stomatal closure [46].
In this review, we will discuss the emerging function of chloroplasts in plant acclimation and adaption to environmental stresses including abiotic and biotic stresses. Our review focuses on findings from the past decade, and highlights the roles of chloroplast metabolites and chloroplast-derived signals in shaping how plants defend against harmful conditions. How chloroplast biology is affected by the changing environment is an emerging area of interest. Together, these studies highlight the important role of the chloroplast in plant adaptation to adverse environmental stresses.

2. Chloroplast Response to Abiotic Stress

Advancing research has shown that chloroplasts play multifaceted roles in the plant response to various types of abiotic stress, including heat, chilling, salt, drought, and high light stresses. Here, we summarize the present state of knowledge on chloroplast responses to various abiotic stresses (Table 1).

2.1. Response to Heat Stress

Leaf photosynthesis is substantially affected by abnormal temperature stresses, including heat stress which is usually 10–15 °C above an optimum temperature for plant growth or chilling stress which occurs in the temperatures range 0–15 °C [27,48]. Chloroplasts play an essential role in activation of physiological adaptive processes to these adverse temperature stresses.
It is reported that the chloroplast is sensitive to high-temperature stress during photosynthesis [48]. Research has revealed a close association between the chloroplast-related genes and high-temperature stress in the model plant rice. The expression of more than two hundred genes was upregulated in response to heat stress [49]. In a series of plant species, heat-induced leaf chlorosis has been observed [48]. After heat treatment, the activities of chlorophyll-degrading enzymes increased significantly, and the activity of key chlorophyll-synthesizing enzymes was unchanged [50]. Studies on genetic variations in hybrids of colonial (Agrostis capillaris) x creeping bentgrass (Agrostis stolonifera) indicated that the rapid breakdown of chlorophyll induced by heat stress was related to activation of genes encoding chlorophyllase and pheophytinase, and pheophytinase (PPH) activity [51]. The stay-green physiological traits were selected to evaluate the heat tolerance of plants and reveal the potential mechanism of heat damage associated with alterations in Chl metabolism and antioxidant and photosynthetic capacity. In creeping bentgrass species, adaptability to high temperature and stay-green genotypes was highly associated with chlorophyll metabolism [52]. Stay-green (SGR) genes encode magnesium dechelatase, and are involved in chlorophyll (Chl) degradation. Stay-green (SGR) homologs remove magnesium from Chl a, which is one of the most important components in the Chl degradation pathway in plants [53,54,55]. Under high-temperature conditions, accumulation of sugars in the peel was induced in bananas, and these sugars regulated Chl degradation through SGR proteins [56].
A series of research has shown that regulation of the activity of photosynthetic pathway enzyme Rubisco contributes to plant adaption to the heat stress. Rubisco activase (Rca1), a catalytic chaperone involved in modulating the Rubisco activity, plays a role in wheat response to heat stress [57]. The tomato (Solanum lycopersicum) chloroplast-targeted DnaJ protein (SlCDJ2) is located in the thylakoids and stroma of the chloroplasts. When plants respond to heat stress, SlCDJ2 protects Rubisco activity, and contributes to maintenance of CO2 assimilation capacity, which establishes a role for SlCDJ2 in coping with heat stress [58]. The tomato (Lycopersicon esculentum) chloroplast-targeted DnaJ protein (LeCDJ1) also plays a role in plant response to high temperature [59].
Furthermore, the activity of PSI and PSII is severely affected by high-temperature conditions. In A. thaliana, heat stress can modulate the transcript accumulation of the plastid-encoded PSI and PSII genes such as the psaA, psaB, psbA, psbD, and psbN. Furthermore, the regulation is performed in part via the expression of HS-responsive nuclear genes for the plastid transcription machinery [60]. In wheat plants, the increased photosynthetic rate, improved ATPase activity in the thylakoid membrane, and enhanced efficiency of PSII photochemistry, which was achieved by overexpression of the ubiquitin/26S proteasome system TaUb2, contributed to plants coping with high-temperature stress [61]. When plants are exposed to transient heat waves, insufficient PSI photoprotection including the regulation of linear electron transport and the prevention of over-reduction, may affect the wheat photosynthetic capacity and make plants more susceptible to heat stress [62].
When plants were subjected to high-temperature stress, they generated large amounts of ROS and initiated related signaling events to survive the adverse environments [63]. In a recent study, researchers found that, under heat stress, the ROS levels contributed to mitigation of PSII photoinhibition in a coffee crop [64]. When plants respond to heat stress, the chloroplast heat-shock protein (Hsp) 21 becomes associated with the thylakoid membranes and plays a role in plant stress resistance [65].

2.2. Response to Low-Temperature Stress

In addition to high-temperature tolerance, chloroplasts are involved in plant cold-stress response. A series of studies have reported that chloroplasts can also perceive chilling stress signals, promote photosynthesis, and enhance plant resistance to adverse environment stress [27]. Previous and recent studies showed that low-temperature conditions could affect the abundance of various proteins involved in photosynthesis [27]. Through iTRAQ-based proteomic analysis between chilling-tolerant and chilling-sensitive rice lines, scientists revealed the dynamic response of chloroplast photosynthetic proteins under chilling conditions [66]. Systematic analysis of cold-stress response using transcriptome data was performed in rice, and the stay-green (SGR) proteins were identified as hub genes in this life process. Furthermore, SGR proteins were involved in the crosstalk between cold-stress responses and diurnal rhythmic patterns, providing new insights in understanding the plant environmental stress response against climate change [67].
Chilling can affect the structure, function, and development of chloroplasts [68]. Scientists revealed that chilling can induce structural changes during chloroplast biogenesis in cucumber cotyledons [69]. When exposed to low temperatures, plant chloroplasts changed the content of unsaturated fatty acids in chloroplast membranes to increase plant tolerance to the adverse temperatures [70]. When plants adapted to chilling stresses, the activities of chloroplast dark-reaction-related enzyme were also regulated. For instance, the reductive activity of two key enzymes involved in the Calvin cycle, fructose-1,6-diphosphatase (FBPase) and isoheptanone-1,7-diphosphatase (SBPase) was significantly reduced [71]. Low-temperature stress hinders chloroplast development and plant photosynthesis. The rice (Oryza sativa) RNA-binding protein DUA1 is required for RNA editing of the rps8-182 site, and plays a vital role in chloroplast development under low-temperature conditions [72]. The chloroplast gene psbA encodes the key D1 reaction center protein of PSII. Recently, the tomato (Solanum lycopersicum) WHIRLY1 (SlWHY1) was found to be induced by chilling conditions and could upregulate the transcription level of psbA through directly binding to the upstream region of its promoter (the sequence “GTTACCCT”). The increased D1 abundance enhanced plant resistance to photoinhibition caused by chilling stresses [73]. Scientists also found that SlWHY1 could increase the expression level of RbcS1, a member of the Rubisco small-subunit (RBCS) multigene family, and help plants maintain high Rubisco content under low-temperature conditions [74]. Despite the role of chloroplast-targeted DnaJ protein in plant response to heat stress, the function of tomato (Lycopersicon esculentum) chloroplast-targeted DnaJ protein (LeCDJ1) under chilling stress was also investigated. LeCDJ1 showed essential functions in maintaining PSII activity under low-temperature stress [75].
The ROS function has an important retrograde signal in chloroplasts under a series of unfavorable environmental conditions. Chilling stress can regulate the redox state of chloroplasts. When plants respond to chilling stress, the photosynthetic electron transport chain in chloroplasts transfers excess electrons to O2 and causes O2- increase in bermudagrass [76]. In A. thaliana, regulation of chloroplast-to-nucleus ROS signaling is a strategy to promote plants acclimation to cold stress [77]. Researchers revealed that melatonin increases the chilling tolerance of cucumber seedlings through regulating the ROS balance [78]. Scientists have also found that, under chilling stress, exogenous applications of acetylsalicylic acid can enhance the chloroplast antioxidant system activity and thus improve the tolerance of plants under low temperatures [79].
It is reported that the chloroplast RNA-binding protein RBD1 plays a critical role in plant chilling tolerance. RBD1 directly binds to 23S rRNA, and influences 23S rRNA processing in Arabidopsis, which suggests the importance of chloroplast function especially protein translation in coping with chilling stresses [80].

2.3. Response to Salt Stress

The chloroplast also regulates plant response to salt stress. In soybean, salt stress can decrease the chloroplast Rubisco amount, and Rubisco-containing body (RCBs) formation is responsible for this life process [81]. Sugar beet is a highly salt-tolerant plant and is a model for studying salt acclimation in crops. When sugar beets were exposed to salt stress, they could adjust their cellular redox and reactive oxygen species (ROS) network to improve their salinity tolerance [82]. Under salinity stress conditions, plants modulate protein transport into chloroplasts to enhance tolerance to stresses through upregulating the transcription level of the ubiquitin E3 ligase suppressor of PPI1 locus 1 (SP1). SP1 induces degradation of translocon at the outer envelope membrane of chloroplasts (TOC), inhibits photosynthesis, and decreases ROS formation [83,84]. Recently, it has been reported that the chloroplast Hsp70 chaperone protein and Clp protease systems can protect plants from the environmental stress conditions such as salinity-triggered oxidative stress. The Hsp70 chaperone systems refold proteins after stress, while Clp protease degrades the misfolded and aggregated proteins [85]. In cabbage (Brassica rapa), the chloroplast-targeted DEAD-box RNA helicase BrRH22 expression was induced by high salinity or drought stress and by ABA treatment. BrRH22 had the RNA chaperone function and affected chloroplast gene translation, eventually positively regulating plant response to abiotic stress [86]. To some extent, the stay-green (SGR) phenotype protects the plants against abiotic stress conditions. In rice, overexpression transgenic lines of RNA-binding bacterial chaperones encoding genes CspA and CspB displayed a distinct stay-green (SGR) phenotype, higher transcript levels of SGR, and enhanced multiple stress tolerance. This research indicated that bacterial chaperone proteins are capable of imparting SGR phenotype and salt- and drought-stress tolerance alongside grain improvement [87].

2.4. Response to High-Light Stress

Extreme changes in light intensities in the environment are also adverse environmental stresses for plants. When A. thaliana seedlings respond to drought and high light stresses, a SAL1-PAP retrograde pathway in chloroplast can regulate the expression of a subset of high-light and drought-inducible nuclear genes, and enhance their acclimation to these stresses [16]. By analysis of the changes in chloroplast transcript accumulation and translation in leaves of tobacco (Nicotiana tabacum) seedlings after transferring from moderate light to physiological low or high light, scientists found that the transcription level of only a single chloroplast gene psbA were significantly changed, suggesting the limited responsiveness of chloroplast gene expression during adaption to high light in tobacco [88]. When grape leaves responded to the combined stress of high light and high temperature, the cyclic electron flow around PSI was stimulated and played an important role in PSI and PSII photoprotection [89]. During plants’ acclimation to fluctuating light, chloroplasts send information to the nucleus. In Nicotiana benthamiana epidermal cells, high light increased chloroplast H2O2 production, and the produced H2O2 was transferred directly from chloroplasts to nucleus to control nuclear gene expression [90]. The transcriptome of A. thaliana cell suspension culture under high-light conditions was analyzed. Key components of the ROS signaling transduction pathway and transcription factors that regulate ROS scavenging were upregulated during early transcriptional responses to high-light stress [29]. Scientists found that the thylakoid membrane protease FtSH in Chlamydomonas reinhardtii play a vital role in the quality control of thylakoid membrane proteins and in the response to light stress [91].

2.5. Response to Drought Stress

Chloroplasts also play a pivotal role in plant acclimatization to drought stresses [3,7,92]. As mentioned above, when plants respond to drought stress, the SAL1-PAP chloroplast retrograde pathway regulates nuclear stress-responsive genes and stomatal closure to improve plant drought tolerance [16,46]. Drought stress can induce the expression of chloroplast-targeted DEAD-box RNA helicase BrRH22 in cabbage, which regulates plant response to abiotic stress [86]. The rice gene OsCTR1 encodes the RING Ub E3 ligase, and its encoded protein is localized in the chloroplasts. OsCTR1 interacted with two chloroplast-localized proteins OsCP12 and OsRP1. Heterogeneous overexpression of OsCTR1 transgenic Arabidopsis plants was ABA-sensitive and showed improved tolerance against severe water deficits, indicating the involvement of OsCTR1 in plant response to water-deficit stress [93]. Researchers performed RNA-Seq analysis using roots from 4-week-old rice seedlings grown in soil that had been subjected to drought conditions for 2–3 d [94]. They found that rice phytochrome B (OsPhyB) repressed the activity of ascorbate peroxidase and catalyzed mediating reactive-oxygen-species (ROS) processing machinery required for drought tolerance, suggesting the potential significance of OsPhyB for manipulating drought tolerance in rice [94]. Maize mesophyll lipoxygenase ZmLOX6, a vegetative storage protein (VSP), was targeted to chloroplasts by a novel N-terminal transit peptide. Overexpression of ZmLOX6 improved plant drought tolerance. Furthermore, additional storage of nitrogen by ZmLOX6 as a VSP in maize leaves ameliorated the adverse effect of drought on grain yield [95]. The Salsola laricifolia NADP–malic enzyme (NADP–ME) SaNADP–ME4 was found to be located in the chloroplasts and was highly expressed in leaves. SaNADP–ME4 alleviated the chlorophyll content decrease and PSII photochemical efficiency, and enhanced reactive oxygen species scavenging capability. Arabidopsis overexpressing SaNADP–ME4 showed increased drought-stress resistance [96]. Under moderate drought conditions, the B-box (BBX) gene AtBBX21 overexpression can reduce chloroplast electron transport capacity to increase photosynthesis and improve water-use efficiency in potato (Solanum tuberosum) plants. The function of BBX21 was achieved through the interplay with the ABA signaling networks [97]. Sorghum landraces have evolved in drought-prone regions. Recently scientists investigated the genetics of their adaptation through quantitative and population genomics. They found that the stay-green loci played a broad role in the drought adaptation of sorghum [98].

3. Chloroplast Response to Biotic Stress

Under the attack of biotic agents including arthropods, fungi, and bacterial and viral pathogens, damage is caused to the chloroplasts and plant photosynthesis. Recently, the chloroplasts have emerged as pivotal factors to coordinate plant defense against biotic agents (Table 1) [4,15,99,100,101].
The transcriptome data from eight different plant species exposed to biotic damage were analyzed. As previously reported, the plant-hormone-related genes including jasmonic-acid-, salicylic-acid-, and ethylene-responsive genes were upregulated [100]. More importantly, the photosynthesis-related gene expression was universally downregulated, and the downregulation was an adaptive response to biotic attack, suggesting a role of chloroplasts in coordinating plant biotic defense [102]. Researchers revealed that activation of defense by pathogen-associated molecular patterns (PAMPs) leads to a rapid decrease in nonphotochemical quenching (NPQ), and NPQ also influences plant responses of PAMP-triggered immunity. These results indicate that the regulation of chloroplast NPQ is an intrinsic component of the plant’s defense program [103]. In the presence of pathogen infection, chloroplasts send out dynamic tubular extensions called stromules to communicate with nucleus [104,105]. Their communication is accompanied by the accumulation of chloroplast-localized defense protein NRIP1 and H2O2 in the nucleus, indicating the importance of this communication for successful innate immune responses [104]. Recently, the underlying biological mechanism for the life process in which chloroplasts cluster around nuclear and extended stromules was further uncovered. In Nicotiana benthamiana, scientists found that this response can be triggered by activation of pattern-triggered immunity, ETI, or infection with viruses or bacteria and this response is non-cell-autonomous [106].
PP2C is one of the four major classes of the serine/threonine-specific protein phosphatase family. In A. thaliana, the PP2C genes (AtPP2C62 and AtPP2C26) double-mutant plants showed enhancement of plant immunity and resistance to Xanthomonas campestris pv. campestris infection. Furthermore, the AtPP2C62 and AtPP2C26 protein localized to the chloroplast, and catalyzed the dephosphorylation of the photosynthesis-related protein chaperonin-60. This study implied the occurrence of crosstalk between photosynthesis and the plant defense system [107]. The candidates influencing plant life processes related to the formation and maintenance of stromules were also investigated in Nicotiana benthamiana using Xanthomonas campestris pv. vesicatoria type III-secreted effectors. Overexpression of E3 ubiquitin ligase XopL eliminated the formation of stromules and the relocation of chloroplasts to the nucleus, and microtubules played a vital role in stromule extension and dynamics [108].
Wheat-stripe rust is a devastating disease caused by the fungus Puccinia striiformis f. sp tritici (Pst). The WHEAT KINASE START1 (WKS1) gene encodes a serine/threonine kinase and confers partial resistance to Pst. The wheat (Triticum aestivum) WKS1.1 is targeted to the chloroplast and phosphorylates the thylakoid-associated ascorbate peroxidase (tAPX) to reduce its ability to detoxify peroxides [109]. Furthermore, researchers also found WKS1 interacted with and phosphorylated an extrinsic member of PSII PsbO, which resulted to reduced photosynthesis and conferred Pst resistance [110]. The chloroplastic protein thylakoid formation1 (THF1) plays a vital role in maintaining chloroplast homeostasis. THF1 is a negative regulator of cell death, and can be destabilized by the nucleotide-binding/Leu-rich repeat (NB-LRR) protein N’, revealing novel molecular mechanisms linking light and chloroplasts to the induction of cell death in plant immunity [111]. Recently, the function of the rice thylakoid membrane-bound ascorbate peroxidase OsAPX8 in rice tolerance to bacterial blight Xanthomonas oryzae pv. Oryzae was investigated. The overexpression of OsAPX8 could enhance the rice tolerance to bacterial pathogen by regulating H2O2 accumulation [112]. In rice, the phosphorylation of light-harvesting complex II protein LHCB5 enhances broad-spectrum resistance of rice to the blast fungus Magnaporthe oryzae through modulating ROS accumulation in the chloroplasts. This study uncovered an immunity mechanism mediated by phosphorylation of light-harvesting complex II [113].
In Arabidopsis response to nonhost Pseudomonas syringae pathogens, plants lacking the functional redox detoxification system NADPH-dependent thioredoxin reductase C (NTRC) showed enhanced disease susceptibility of nonhost pathogens and elevated JA-mediated signaling pathways. These results suggested NTRC plays a key role in plant immunity by regulating chloroplast-generated reactive oxygen species [114]. The Arabidopsis pathogen-responsive mitogen-activated protein kinases (MPKs) MPK3 and MPK6 play important roles in promoting plant defense against pathogens. When plants respond to P. syringae pv tomato, the MPK3/MPK6 protein manipulated plant photosynthetic activities and promoted ROS accumulation in chloroplasts, and eventually contributed to the robustness of ETI pathway [115].
The genome-wide expression changes were examined in Arabidopsis leaves following challenge with P. syringae pv tomato DC3000. Scientists found that suppression of chloroplast-associated genes represented a rapid MAMP-triggered defense response, further suggesting the key role of chloroplasts in plant defense [116]. The N-terminal regions of P. syringae pv. tomato DC3000 type-III effector HopK1 represented a chloroplast transit peptide, indicating that the type-III effectors targeted the chloroplasts and the targets within this organelle were important for immunity [117]. The bacterial pathogen P. syringae pv tomato DC3000 cysteine protease effector HopN1 localized to chloroplasts, degraded the oxygen evolving complex of photosystem II PsbQ, and inhibited PSII activity in chloroplast preparations, indicating that PsbQ was a target for pathogen suppression and contributed to plant immunity responses [118]. Upon P. syringae pv tomato DC3000 challenge, virus-induced gene-silenced SlALC and Arabidopsis thf1 mutants exhibited accelerated lesion formation, and SlALC1 chloroplast localization was affected by coronatine [119].
Recently, the role of chloroplastic ROS in plant defense against a typical necrotrophic fungus Botrytis cinerea was investigated. A series of experiments in transgenic Nicotiana tabacum (tobacco) lines expressing a plastid-targeted cyanobacterial flavodoxin (pfld lines) indicated that chloroplast-generated ROS play a major role in lesion development during Botrytis infection. Modulation of chloroplastic ROS levels by the overexpression of a heterologous antioxidant protein can also protect plants against the canonical necrotrophic fungus B. cinerea [120].
Ralstonia solanacearum, a soilborne plant pathogen, invades host plant roots from the soil. This plant pathogen injects type III effector proteins called Rips (Ralstonia-injected proteins) into plant cells. Scientists found that R. solanacearum RipAL localized to chloroplasts and targeted chloroplast lipids. R. solanacearum RipAL induced JA production and suppressed SA-signaling-mediated defense response in plant cells [121]. In wheat, the necrotrophic pathogens Stagonospora nodorum and Pyrenophora tritici-repentis could produce effector ToxA, and wheat sensitivity to ToxA was uniquely governed by the Tsn1 gene. The expression level of Tsn1 was tightly regulated by the circadian clock and light, indicating that Tsn1-ToxA interactions are associated with photosynthesis pathways [122]. The Irish potato famine pathogen Phytophthora infestans secretes the effector protein AVRvnt1, and this protein can be recognized by the nucleotide-binding leucine-rich repeat (NLR) protein Rpi-vnt1.1. In the dark, Rpi-vnt1.1-mediated resistance was compromised, indicating that pathogens manipulated the chloroplast function and resulted in a light-dependent immune response [123]. SsITL is an effector protein of the necrotrophic phytopathogen Sclerotinia sclerotiorum, and suppresses host immunity at the early stage of infection. Recently, scientists found that SsITL interacted with a chloroplast-localized calcium-sensing receptor CAS, interfered with the plant salicylic acid (SA) signaling pathway, and facilitated the infection by S. sclerotiorum [124].
Table
Table 1. Summary of known chloroplast biological processes involved in plant stress response.
Table 1. Summary of known chloroplast biological processes involved in plant stress response.
ComponentsSpeciesProcess/StimulusMolecular FunctionReference
Heat stress
SGRMusa acuminataChlorophyll degradationStay-green protein[56]
Rca1Triticum aestivumModulate the activity of RubiscoA catalytic chaperone[57]
CDJ2Solanum lycopersicum,
Lycopersicon esculentum		Protect Rubisco activityChloroplast-targeted DnaJ protein[58,59]
Ub2Triticum aestivumImprove antioxidant capacityUbiquitin/26S proteasome system[61]
Hsp21Arabidopsis thalianaAssociate with the thylakoid membranesSmall heat-shock protein chaperone[65]
Chilling stress
FBPase, SBPaseZea mays L.Compensate for decreases in photosynthetic capacityEnzymes involved in the Calvin cycle[71]
DUA1Oryza sativaRegulate chloroplast developmentRNA-binding protein[72]
WHY1Solanum lycopersicumUpregulate the PSII key D1 reaction center protein encoding gene psbA; maintain high Rubisco contentWHIRLY proteins—the plant-specific DNA-binding proteins[73,74]
CDJ1Lycopersicon esculentumMaintain PSII activityChloroplast-targeted DnaJ protein[75]
RBD1Arabidopsis thalianaRegulate chloroplast protein translation by influencing 23S rRNA processingChloroplast RNA-binding protein[80]
Salt stress
SP1Arabidopsis thalianaInduce the degradation of translocon at the outer envelope membrane of chloroplasts (TOC)Uiquitin E3 ligase suppressor of PPI1 locus 1[83,84]
Hsp70,
Clp protease		Arabidopsis thalianaProtect plants from salinity-triggered oxidative stressHsp70—chaperone;
Clp—a protease system		[85]
RH22Brassica rapaAffect chloroplast gene translationCloroplast-targeted DEAD-box RNA helicase[86]
CspA, CspBOryza sativaImpart SGR phenotypeRNA-binding bacterial chaperones[87]
High-light stress
SAL1-PAPArabidopsis thalianaRegulate stress-inducible nuclear genesComponents of retrograde pathway[16]
FtSHChlamydomonas reinhardtiiControl the quality of thylakoid membrane proteinsThylakoid membrane protease[91]
Drought stress
SAL1-PAPArabidopsis thalianaRegulate the stress-inducible nuclear genesComponents of retrograde pathway[16]
RH22Brassica rapaAffect chloroplast genes’ translationChloroplast-targeted DEAD-box RNA helicase[86]
CTR1Oryza sativaInteract with two chloroplast-localized proteins, OsCP12 and OsRP1RING Ub E3 ligase[93]
PhyBOryza sativaRepress the activity of ascorbate peroxidasePhytochrome B[94]
LOX6Zea maysAdditional storage of nitrogenMesophyll lipoxygenase in chloroplast[95]
NADP-ME4Salsola laricifoliaAlleviate chlorophyll content decrease and PSII photochemical efficiencyNADP-malic enzyme[96]
BBX21Solanum tuberosumReduce chloroplast electron transport capacityB-box (BBX) protein[97]
Biotic stress
PP2C62, PP2C26Arabidopsis thalianaCatalyze the dephosphorylation of the photosynthesis-related protein, chaperonin-60Components of the serine/threonine-specific protein phosphatase family[107]
XopLNicotiana benthamianaEliminate stromules formation and chloroplast relocationE3 ubiquitin ligase[108]
WKS1Triticum aestivumPhosphorylate thylakoid-associated ascorbate peroxidase (tAPX) and detoxify peroxides; phosphorylate an extrinsic member of photosystem II (PSII) PsbOA serine/threonine kinase[109,110]
THF1Nicotiana benthamianaMaintain chloroplast homeostasisChloroplastic protein thylakoid formation1[111]
APX8Oryza sativaRegulate H2O2 accumulationThylakoid membrane-bound ascorbate peroxidase[112]
LHCB5Oryza sativaRegulate ROS accumulationLight-harvesting complex II protein[113]
NTRCArabidopsis thalianaModulate chloroplast-generated ROSRedox detoxification system NADPH-dependent thioredoxin reductase C[114]
MPK3, MPK6Arabidopsis thalianaManipulate plant photosynthetic activities and promote ROS accumulationMitogen-activated protein kinase[115]
PsbQNicotiana benthamiana, Arabidopsis thalianaA target for pathogen suppression and contributes to plant immunity responsesThe oxygen evolving complex of photosystem II[118]
ALCSolanum lycopersicum, Arabidopsis thalianaRegulate disease-associated necrotic cell deathChloroplast genes with altered responses to coronatine[119]
RipALRalstonia solanacearumLocalized to chloroplasts and targeted chloroplast lipidsType III effector proteins[121]
Tsn1Triticum aestivumInteract with effector protein ToxAA unique wheat disease resistance-like gene, regulated by the circadian clock and light[122]
Rpi-vnt1.1Nicotiana benthamianaRecognize the effector protein AVRvnt1, and mediate a light-dependent immune responseA nucleotide-binding leucine-rich repeat (NLR) protein[123]
CASArabidopsis thalianaRecognize the effector protein, and interfere with the salicylic acid (SA) signaling pathwayA chloroplast-localized calcium-sensing receptor[124]

4. Conclusions and Future Perspectives

Adverse environmental stresses greatly influence plant growth and development. Photosynthesis, one of the most important anabolic processes in plants, is severely inhibited by adverse conditions.
In crop species, the reduced photosynthesis rate under adverse environmental conditions eventually causes severe yield and economic losses. It is well known that the chloroplast is a unique organelle in green plant cells for hosting photosynthesis. Recent studies, as summarized in this review, have indicated that chloroplasts also act as sensors of external environment stresses and communicate via a series of retrograde signals to the nucleus, and thus they play an essential role in plant response to abiotic and biotic stresses.
In recent decades, extraordinary progress has been made in the field of elucidating the role of the chloroplast in the plant’s response to abiotic and biotic stresses. To facilitate plant survival under adverse environmental stresses, chloroplasts regulate their structure, gene expression, protein remodeling, and the related metabolic pathways including chloroplast-sourced oxylipins, hormones, hydrogen peroxide, and singlet oxygen. However, future challenges in this field are complex and multiple. First, whether the responses in chloroplasts are inevitable consequences of adverse environmental-stress induction and whether these responses have certain roles in inducing plant tolerance to stress damage. Second, how environmental stresses trigger chloroplast response. Third, how chloroplast responses are transferred out of the chloroplast and induce multiple retrograde signaling pathways to communicate with the nucleus. Finally, whether the present retrograde signaling pathways from the chloroplast to the nucleus under stress conditions are mainly related to reactive oxygen species, and whether other retrograde signaling pathways are involved in the chloroplast’s response to stresses needs further investigation. Dissection of these questions will help understanding of the precise function of chloroplasts in the plant stress response and lay the foundation for genetically improving plant-stress resilience.

Author Contributions

M.R. conceived and planned this review paper. Y.S. and L.F. prepared and drafted the manuscript. M.A.M.A., A.J. and M.R. revised the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by grants from the National Natural Science Foundation of China (U1804231, 31972469, 31672206), the State Key Laboratory of Cotton Biology Open Fund (CB2021A15), the Agricultural Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences (34-IUA-02), the Sichuan Science and Technology Program (2020JDRC0044), and local financial funds of the National Agricultural Science & Technology Center (NASC), Chengdu (NASC2020AR08; NASC2021KR03).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Zhu, J.K. Abiotic Stress Signaling and Responses in Plants. Cell 2016, 167, 313–324. [Google Scholar] [CrossRef] [Green Version]
  2. Fedoroff, N.V.; Battisti, D.S.; Beachy, R.N.; Cooper, P.J.; Fischhoff, D.A.; Hodges, C.N.; Knauf, V.C.; Lobell, D.; Mazur, B.J.; Molden, D.; et al. Radically Rethinking Agriculture for the 21st Century. Science 2010, 327, 833–834. [Google Scholar] [CrossRef] [Green Version]
  3. Zhang, Y.; Zhang, A.; Li, X.; Lu, C. The Role of Chloroplast Gene Expression in Plant Responses to Environmental Stress. Int. J. Mol. Sci. 2020, 21, 6082. [Google Scholar] [CrossRef]
  4. Littlejohn, G.R.; Breen, S.; Smirnoff, N.; Grant, M. Chloroplast Immunity Illuminated. New Phytol. 2021, 229, 3088–3107. [Google Scholar] [CrossRef]
  5. Serrano, I.; Audran, C.; Rivas, S. Chloroplasts at Work During Plant Innate Immunity. J. Exp. Bot. 2016, 67, 3845–3854. [Google Scholar] [CrossRef]
  6. Mamaeva, A.; Taliansky, M.; Filippova, A.; Love, A.J.; Golub, N.; Fesenko, I. The Role of Chloroplast Protein Remodeling in Stress Responses and Shaping of The Plant Peptidome. New Phytol. 2020, 227, 1326–1334. [Google Scholar] [CrossRef]
  7. Watson, S.J.; Sowden, R.G.; Jarvis, P. Abiotic Stress-induced Chloroplast Proteome Remodelling: A Mechanistic Overview. J. Exp. Bot. 2018, 69, 2773–2781. [Google Scholar] [CrossRef]
  8. Bose, J.; Munns, R.; Shabala, S.; Gilliham, M.; Pogson, B.; Tyerman, S.D. Chloroplast Function and Ion Regulation in Plants Growing on Saline Soils: Lessons from Halophytes. J. Exp. Bot. 2017, 68, 3129–3143. [Google Scholar] [CrossRef]
  9. Daniell, H.; Lin, C.S.; Yu, M.; Chang, W.J. Chloroplast Genomes: Diversity, Evolution, and Applications in Genetic Engineering. Genome Biol. 2016, 17, 134. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  10. Huo, Y.; Gao, L.; Liu, B.; Yang, Y.; Kong, S.; Sun, Y.; Yang, Y.; Wu, X. Complete Chloroplast Genome Sequences of Four Allium Species: Comparative and Phylogenetic Analyses. Sci. Rep. 2019, 9, 12250. [Google Scholar] [CrossRef] [Green Version]
  11. Chan, K.X.; Phua, S.Y.; Crisp, P.; McQuinn, R.; Pogson, B.J. Learning the Languages of the Chloroplast: Retrograde Signaling and Beyond. Annu. Rev. Plant Biol. 2016, 67, 25–53. [Google Scholar] [CrossRef]
  12. Crawford, T.; Lehotai, N.; Strand, Å. The Role of Retrograde Signals during Plant Stress Responses. J. Exp. Bot. 2018, 69, 2783–2795. [Google Scholar] [CrossRef]
  13. de Souza, A.; Wang, J.Z.; Dehesh, K. Retrograde Signals: Integrators of Interorganellar Communication and Orchestrators of Plant Development. Annu. Rev. Plant Biol. 2017, 6, 85–108. [Google Scholar] [CrossRef]
  14. Wu, G.Z.; Meyer, E.H.; Wu, S.; Bock, R. Extensive Posttranscriptional Regulation of Nuclear Gene Expression by Plastid Retrograde Signals. Plant Physiol. 2019, 180, 2034–2048. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  15. Fernandez, J.C.; Burch-Smith, T.M. Chloroplasts as Mediators of Plant Biotic Interactions over Short and Long Distances. Curr. Opin. Plant Biol. 2019, 50, 148–155. [Google Scholar] [CrossRef]
  16. Estavillo, G.M.; Crisp, P.A.; Pornsiriwong, W.; Wirtz, M.; Collinge, D.; Carrie, C.; Giraud, E.; Whelan, J.; David, P.; Javot, H.; et al. Evidence for A SAL1-PAP Chloroplast Retrograde Pathway that Functions in Drought and High Light Signaling in Arabidopsis. Plant Cell 2011, 23, 3992–4012. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  17. Häusler, R.E.; Heinrichs, L.; Schmitz, J.; Flügge, U.I. How Sugars might Coordinate Chloroplast and Nuclear Gene Expression during Acclimation to High Light Intensities. Mol. Plant 2014, 7, 1121–1137. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  18. Ramel, F.; Birtic, S.; Ginies, C.; Soubigou-Taconnat, L.; Triantaphylidès, C.; Havaux, M. Carotenoid Oxidation Products are Stress Signals that Mediate Gene Responses to Singlet Oxygen in Plants. Proc. Natl. Acad. Sci. USA 2012, 109, 5535–5540. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  19. Shumbe, L.; Bott, R.; Havaux, M. Dihydroactinidiolide, a High Light-Induced β-carotene Derivative that Can Regulate Gene Expression and Photoacclimation in Arabidopsis. Mol. Plant 2014, 7, 1248–1251. [Google Scholar] [CrossRef] [Green Version]
  20. Strand, A.; Asami, T.; Alonso, J.; Ecker, J.R.; Chory, J. Chloroplast to Nucleus Communication Triggered by Accumulation of Mg-protoporphyrinIX. Nature 2003, 421, 79–83. [Google Scholar] [CrossRef] [PubMed]
  21. Vogel, M.O.; Moore, M.; König, K.; Pecher, P.; Alsharafa, K.; Lee, J.; Dietz, K.J. Fast Retrograde Signaling in Response to High Light Involves Metabolite Export, MITOGEN-ACTIVATED PROTEIN KINASE6, and AP2/ERF Transcription Factors in Arabidopsis. Plant Cell 2014, 26, 1151–1165. [Google Scholar] [CrossRef] [Green Version]
  22. Woodson, J.D.; Perez-Ruiz, J.M.; Schmitz, R.J.; Ecker, J.R.; Chory, J. Sigma Factor-Mediated Plastid Retrograde Signals Control Nuclear Gene Expression. Plant J. 2013, 73, 1–13. [Google Scholar] [CrossRef] [Green Version]
  23. Xiao, Y.; Savchenko, T.; Baidoo, E.E.; Chehab, W.E.; Hayden, D.M.; Tolstikov, V.; Corwin, J.A.; Kliebenstein, D.J.; Keasling, J.D.; Dehesh, K. Retrograde Signaling by the Plastidial Metabolite MEcPP Regulates Expression of Nuclear Stress-response Genes. Cell 2012, 149, 1525–1535. [Google Scholar] [CrossRef] [Green Version]
  24. Mignolet-Spruyt, L.; Xu, E.; Idänheimo, N.; Hoeberichts, F.A.; Mühlenbock, P.; Brosché, M.; Van Breusegem, F.; Kangasjärvi, J. Spreading the News: Subcellular and Organellar Reactive Oxygen Species Production and Signalling. J. Exp. Bot. 2016, 67, 3831–3844. [Google Scholar] [CrossRef] [Green Version]
  25. Tripathy, B.C.; Oelmüller, R. Reactive Oxygen Species Generation and Signaling in Plants. Plant Signal Behav. 2012, 7, 1621–1633. [Google Scholar] [CrossRef]
  26. Chan, K.X.; Crisp, P.A.; Estavillo, G.M.; Pogson, B.J. Chloroplast-to-Nucleus Communication: Current Knowledge, Experimental Strategies and Relationship to Drought Stress Signaling. Plant Signal Behav. 2010, 5, 1575–1582. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  27. Gan, P.; Liu, F.; Li, R.; Wang, S.; Luo, J. Chloroplasts- Beyond Energy Capture and Carbon Fixation: Tuning of Photosynthesis in Response to Chilling Stress. Int. J. Mol. Sci. 2019, 20, 5046. [Google Scholar] [CrossRef] [Green Version]
  28. Triantaphylidès, C.; Havaux, M. Singlet Oxygen in Plants: Production, Detoxification and Signaling. Trends Plant Sci. 2009, 14, 219–228. [Google Scholar] [CrossRef]
  29. González-Pérez, S.; Gutiérrez, J.; García-García, F.; Osuna, D.; Dopazo, J.; Lorenzo, Ó.; Revuelta, J.L.; Arellano, J.B. Early Transcriptional Defense Responses in Arabidopsis Cell Suspension Culture under High-Light Conditions. Plant Physiol. 2011, 156, 1439–1456. [Google Scholar] [CrossRef] [Green Version]
  30. Meskauskiene, R.; Nater, M.; Goslings, D.; Kessler, F.; Op den Camp, R.; Apel, K.F.L.U. A Negative Regulator of Chlorophyll Biosynthesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 2001, 98, 12826–12831. [Google Scholar] [CrossRef] [Green Version]
  31. Wagner, D.; Przybyla, D.; Op den Camp, R.; Kim, C.; Landgraf, F.; Lee, K.P.; Würsch, M.; Laloi, C.; Nater, M.; Hideg, E.; et al. The Genetic Basis of Singlet Oxygen-Induced Stress Responses of Arabidopsis thaliana. Science 2004, 306, 1183–1185. [Google Scholar] [CrossRef] [PubMed]
  32. Op den Camp, R.G.; Przybyla, D.; Ochsenbein, C.; Laloi, C.; Kim, C.; Danon, A.; Wagner, D.; Hideg, E.; Göbel, C.; Feussner, I.; et al. Rapid Induction of Distinct Stress Responses After the Release of Singlet Oxygen in Arabidopsis. Plant Cell 2003, 15, 2320–2332. [Google Scholar] [CrossRef] [Green Version]
  33. Page, M.T.; McCormac, A.C.; Smith, A.G.; Terry, M.J. Singlet Oxygen Initiates a Plastid Signal Controlling Photosynthetic Gene Expression. New Phytol. 2017, 213, 1168–1180. [Google Scholar] [CrossRef] [PubMed]
  34. Lee, K.P.; Kim, C.; Landgraf, F.; Apel, K. EXECUTER1- and EXECUTER2-Dependent Transfer of Stress-Related Signals from the Plastid to the Nucleus of Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 2007, 104, 10270–10275. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  35. Kim, C.; Apel, K. Singlet Oxygen-Mediated Signaling in Plants: Moving from Flu to Wild Type Reveals an Increasing Complexity. Photosynth. Res. 2013, 116, 455–464. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  36. Uberegui, E.; Hall, M.; Lorenzo, Ó.; Schröder, W.P.; Balsera, M. An Arabidopsis Soluble Chloroplast Proteomic Analysis Reveals the Participation of the Executer Pathway in Response to Increased Light Conditions. J. Exp. Bot. 2015, 66, 2067–2077. [Google Scholar] [CrossRef] [Green Version]
  37. Carmody, M.; Crisp, P.A.; d’Alessandro, S.; Ganguly, D.; Gordon, M.; Havaux, M.; Albrecht-Borth, V.; Pogson, B.J. Uncoupling High Light Responses from Singlet Oxygen Retrograde Signaling and Spatial-Temporal Systemic Acquired Acclimation. Plant Physiol. 2016, 171, 1734–1749. [Google Scholar] [CrossRef] [Green Version]
  38. Wang, L.; Kim, C.; Xu, X.; Piskurewicz, U.; Dogra, V.; Singh, S.; Mahler, H.; Apel, K. Singlet Oxygen- and EXECUTER1-Mediated Signaling Is Initiated in Grana Margins and Depends on the Protease FtsH2. Proc. Natl. Acad. Sci. USA 2016, 113, E3792–E3800. [Google Scholar] [CrossRef] [Green Version]
  39. Dogra, V.; Duan, J.; Lee, K.P.; Lv, S.; Liu, R.; Kim, C. FtsH2-Dependent Proteolysis of EXECUTER1 Is Essential in Mediating Singlet Oxygen-Triggered Retrograde Signaling in Arabidopsis thaliana. Front Plant Sci. 2017, 8, 1145. [Google Scholar] [CrossRef] [Green Version]
  40. Shumbe, L.; D’Alessandro, S.; Shao, N.; Chevalier, A.; Ksas, B.; Bock, R.; Havaux, M. METHYLENE BLUE SENSITIVITY 1 (MBS1) is Required for Acclimation of Arabidopsis to Singlet Oxygen and Acts Downstream of β-cyclocitral. Plant Cell Environ. 2017, 40, 216–226. [Google Scholar] [CrossRef] [Green Version]
  41. Maruta, T.; Noshi, M.; Tanouchi, A.; Tamoi, M.; Yabuta, Y.; Yoshimura, K.; Ishikawa, T.; Shigeoka, S. H2O2-Triggered Retrograde Signalingfrom Chloroplasts to Nucleus Plays Specific Role in Response to Stress. J. Biol. Chem. 2012, 287, 11717–11729. [Google Scholar] [CrossRef] [Green Version]
  42. Petrov, V.D.; Van Breusegem, F. Hydrogen Peroxide-A Central Hub for Information Flow in Plant Cells. AoB Plants 2012, 2012, pls014. [Google Scholar] [CrossRef] [Green Version]
  43. Benn, G.; Bjornson, M.; Ke, H.; De Souza, A.; Balmond, E.I.; Shaw, J.T.; Dehesh, K. Plastidial Metabolite MEcPP Induces a Transcriptionally Centered Stress-response Hub Via the Transcription Factor CAMTA3. Proc. Natl. Acad. Sci. USA 2016, 113, 8855–8860. [Google Scholar] [CrossRef] [Green Version]
  44. Walley, J.; Xiao, Y.; Wang, J.Z.; Baidoo, E.E.; Keasling, J.D.; Shen, Z.; Briggs, S.P.; Dehesh, K. Plastid-Produced Interorgannellar Stress Signal MEcPP Potentiates Induction of the Unfolded Protein Response in Endoplasmic Reticulum. Proc. Natl. Acad. Sci. USA 2015, 112, 6212–6217. [Google Scholar] [CrossRef] [Green Version]
  45. Lemos, M.; Xiao, Y.; Bjornson, M.; Wang, J.Z.; Hicks, D.; Souza, A.; Wang, C.Q.; Yang, P.; Ma, S.; Dinesh-Kumar, S.; et al. The Plastidial Retrograde Signal Methyl Erythritol Cyclopyrophosphate Is a Regulator of Salicylic Acid and Jasmonic Acid Crosstalk. J. Exp. Bot. 2016, 67, 1557–1566. [Google Scholar] [CrossRef] [Green Version]
  46. Pornsiriwong, W.; Estavillo, G.M.; Chan, K.X.; Tee, E.E.; Ganguly, D.; Crisp, P.A.; Phua, S.Y.; Zhao, C.; Qiu, J.; Park, J.; et al. A Chloroplast Retrograde Signal, 3’-Phosphoadenosine 5’-Phosphate, Acts as A Secondary Messenger in Abscisic Acid Signaling in Stomatal Closure and Germination. eLife 2017, 6, e23361. [Google Scholar] [CrossRef]
  47. Chan, K.X.; Mabbitt, P.D.; Phua, S.Y.; Mueller, J.W.; Nisar, N.; Gigolashvili, T.; Stroeher, E.; Grassl, J.; Arlt, W.; Estavillo, G.M.; et al. Sensing and Signaling of Oxidative Stress in Chloroplasts by Inactivation of the SAL1 Phosphoadenosine Phosphatase. Proc. Natl. Acad. Sci. USA 2016, 113, E4567–E4576. [Google Scholar] [CrossRef] [Green Version]
  48. Wang, Q.L.; Chen, J.H.; He, N.Y.; Guo, F.Q. Metabolic Reprogramming in Chloroplasts under Heat Stress in Plants. Int. J. Mol. Sci. 2018, 19, 849. [Google Scholar] [CrossRef] [Green Version]
  49. Yoo, Y.H.; Hong, W.J.; Jung, K.H. A Systematic View Exploring the Role of Chloroplasts in Plant Abiotic Stress Responses. Biomed. Res Int. 2019, 2019, 6534745. [Google Scholar] [CrossRef]
  50. Rossi, S.; Burgess, P.; Jespersen, D.; Huang, B. Heat-Induced Leaf Senescence Associated with Chlorophyll Metabolism in Bentgrass Lines Differing in Heat Tolerance. Crop Sci. 2017, 57, S169–S178. [Google Scholar] [CrossRef]
  51. Jespersen, D.; Zhang, J.; Huang, B. Chlorophyll Loss Associated with Heat-induced Senescence in Bentgrass. Plant Sci. 2016, 249, 1–12. [Google Scholar] [CrossRef]
  52. Li, Z.; Tang, M.; Hassan, M.J.; Zhang, Y.; Han, L.; Peng, Y. Adaptability to High Temperature and Stay-Green Genotypes Associated with Variations in Antioxidant, Chlorophyll Metabolism, and γ-Aminobutyric Acid Accumulation in Creeping Bentgrass Species. Front. Plant Sci. 2021, 12, 750728. [Google Scholar] [CrossRef]
  53. Jiao, B.; Meng, Q.; Lv, W. Roles of Stay-green (SGR) Homologs during Chlorophyll Degradation in Green Plants. Bot. Stud. 2020, 61, 25. [Google Scholar] [CrossRef]
  54. Ono, K.; Kimura, M.; Matsuura, H.; Tanaka, A.; Ito, H. Jasmonate Production through Chlorophyll A Degradation by Stay-Green in Arabidopsis thaliana. J. Plant Physiol. 2019, 238, 53–62. [Google Scholar] [CrossRef]
  55. Shimoda, Y.; Ito, H.; Tanaka, A. Arabidopsis STAY-GREEN, Mendel’s Green Cotyledon Gene, Encodes Magnesium-Dechelatase. Plant Cell 2016, 28, 2147–2160. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  56. Yang, X.; Pang, X.; Xu, L.; Fang, R.; Huang, X.; Guan, P.; Lu, W.; Zhang, Z. Accumulation of Soluble Sugars in Peel at High Temperature Leads to Stay-green Ripe Banana Fruit. J. Exp. Bot. 2009, 60, 4051–4062. [Google Scholar] [CrossRef]
  57. Kumar, R.R.; Goswami, S.; Singh, K.; Dubey, K.; Singh, S.; Sharma, R.; Verma, N.; Kala, Y.K.; Rai, G.K.; Grover, M.; et al. Identification of Putative RuBisCo Activase (TaRca1)-The Catalytic Chaperone Regulating Carbon Assimilatory Pathway in Wheat (Triticum aestivum) under the Heat Stress. Front. Plant Sci. 2016, 7, 986. [Google Scholar] [CrossRef] [Green Version]
  58. Wang, G.; Kong, F.; Zhang, S.; Meng, X.; Wang, Y.; Meng, Q. A Tomato Chloroplast-Targeted DnaJ Protein Protects Rubisco Activity under Heat Stress. J. Exp. Bot. 2015, 66, 3027–3040. [Google Scholar] [CrossRef] [Green Version]
  59. Kong, F.; Deng, Y.; Wang, G.; Wang, J.; Liang, X.; Meng, Q. LeCDJ1, A Chloroplast DnaJ Protein, Facilitates Heat Tolerance in Transgenic Tomatoes. J. Integr. Plant Biol. 2014, 56, 63–74. [Google Scholar] [CrossRef] [PubMed]
  60. Danilova, M.N.; Kudryakova, N.V.; Andreeva, A.A.; Doroshenko, A.S.; Pojidaeva, E.S.; Kusnetsov, V.V. Differential Impact of Heat Stress on the Expression of Chloroplast-Encoded Genes. Plant Physiol. Biochem. 2018, 129, 90–100. [Google Scholar] [CrossRef]
  61. Tian, F.; Gong, J.; Zhang, J.; Feng, Y.; Wang, G.; Guo, Q.; Wang, W. Overexpression of Monoubiquitin Improves Photosynthesis in Transgenic Tobacco Plants Following High Temperature Stress. Plant Sci. 2014, 226, 92–100. [Google Scholar] [CrossRef]
  62. Chovancek, E.; Zivcak, M.; Botyanszka, L.; Hauptvogel, P.; Yang, X.; Misheva, S.; Hussain, S.; Brestic, M. Transient Heat Waves May Affect the Photosynthetic Capacity of Susceptible Wheat Genotypes Due to Insufficient Photosystem I Photoprotection. Plants 2019, 8, 282. [Google Scholar] [CrossRef] [Green Version]
  63. Vacca, R.A.; Valenti, D.; Bobba, A.; Merafina, R.S.; Passarella, S.; Marra, E. Cytochrome C is Released in a Reactive Oxygen Species-Dependent Manner and is Degraded Via Caspase-like Proteases in Tobacco Bright-Yellow 2 Cells En Route to Heat Shock-Induced Cell Death. Plant Physiol. 2006, 141, 208–219. [Google Scholar] [CrossRef] [Green Version]
  64. Martins, M.Q.; Rodrigues, W.P.; Fortunato, A.S.; Leitão, A.E.; Rodrigues, A.P.; Pais, I.P.; Martins, L.D.; Silva, M.J.; Reboredo, F.H.; Partelli, F.L.; et al. Protective Response Mechanisms to Heat Stress in Interaction with High [CO2] Conditions in Coffea spp. Front Plant Sci. 2016, 7, 947. [Google Scholar] [CrossRef] [Green Version]
  65. Bernfur, K.; Rutsdottir, G.; Emanuelsson, C. The Chloroplast-Localized Small Heat Shock Protein Hsp21 Associates with the Thylakoid Membranes in Heat-Stressed Plants. Protein Sci. 2017, 26, 1773–1784. [Google Scholar] [CrossRef] [PubMed]
  66. Cen, W.; Liu, J.; Lu, S.; Jia, P.; Yu, K.; Han, Y.; Li, R.; Luo, J. Comparative Proteomic Analysis of QTL CTS-12 Derived from Wild Rice (Oryza rufipogon Griff.), in the Regulation of Cold Acclimation and De-Acclimation of Rice (Oryza sativa L.) in Response to Severe Chilling Stress. BMC Plant Biol. 2018, 18, 163. [Google Scholar] [CrossRef]
  67. Hong, W.J.; Jiang, X.; Ahn, H.R.; Choi, J.; Kim, S.R.; Jung, K.H. Systematic Analysis of Cold Stress Response and Diurnal Rhythm Using Transcriptome Data in Rice Reveals the Molecular Networks Related to Various Biological Processes. Int. J. Mol. Sci. 2020, 21, 6872. [Google Scholar] [CrossRef]
  68. Liu, X.; Zhou, Y.; Xiao, J.; Bao, F. Effects of Chilling on the Structure, Function and Development of Chloroplasts. Front. Plant Sci. 2018, 9, 1715. [Google Scholar] [CrossRef] [Green Version]
  69. Skupień, J.; Wójtowicz, J.; Kowalewska, Ł.; Mazur, R.; Garstka, M.; Gieczewska, K.; Mostowska, A. Dark-Chilling Induces Substantial Structural Changes and Modifies Galactolipid and Carotenoid Composition During Chloroplast Biogenesis in Cucumber (Cucumis sativus L.) Cotyledons. Plant Physiol. Biochem. 2017, 111, 107–118. [Google Scholar] [CrossRef]
  70. Xue, M.; Guo, T.; Ren, M.; Wang, Z.; Tang, K.; Zhang, W.; Wang, M. Constitutive Expression of Chloroplast Glycerol-3-Phosphate Acyltransferase from Ammopiptanthus Mongolicus Enhances Unsaturation of Chloroplast Lipids and Tolerance to Chilling, Freezing and Oxidative Stress in Transgenic Arabidopsis. Plant Physiol. Biochem. 2019, 143, 375–387. [Google Scholar] [CrossRef] [PubMed]
  71. Kingston-Smith, A.H.; Harbinson, J.; Williams, J.; Foyer, C.H. Effect of Chilling on Carbon Assimilation, Enzyme Activation, and Photosynthetic Electron Transport in the Absence of Photoinhibition in Maize Leaves. Plant Physiol. 1997, 114, 1039–1046. [Google Scholar] [CrossRef] [Green Version]
  72. Cui, X.; Wang, Y.; Wu, J.; Han, X.; Gu, X.; Lu, T.; Zhang, Z. The RNA Editing Factor DUA1 is Crucial to Chloroplast Development at Low Temperature in Rice. New Phytol. 2019, 221, 834–849. [Google Scholar] [CrossRef] [Green Version]
  73. Zhuang, K.; Kong, F.; Zhang, S.; Meng, C.; Yang, M.; Liu, Z.; Wang, Y.; Ma, N.; Meng, Q. Whirly1 Enhances Tolerance to Chilling Stress in Tomato via Protection of Photosystem II and Regulation of Starch Degradation. New Phytol. 2019, 221, 1998–2012. [Google Scholar] [CrossRef]
  74. Zhuang, K.; Wang, J.; Jiao, B.; Chen, C.; Zhang, J.; Ma, N.; Meng, Q. WHIRLY1 Maintains Leaf Photosynthetic Capacity in Tomato by Regulating the Expression of RbcS1 Under Chilling Stress. J. Exp. Bot. 2020, 71, 3653–3663. [Google Scholar] [CrossRef]
  75. Kong, F.; Deng, Y.; Zhou, B.; Wang, G.; Wang, Y.; Meng, Q. A Chloroplast-Targeted DnaJ Protein Contributes to Maintenance of Photosystem II under Chilling Stress. J. Exp. Bot. 2014, 65, 143–158. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  76. Shi, H.; Ye, T.; Zhong, B.; Liu, X.; Chan, Z. Comparative Proteomic and Metabolomic Analyses Reveal Mechanisms of Improved Cold Stress Tolerance in Bermudagrass (Cynodon dactylon (L.) Pers.) by Exogenous Calcium. J. Integr. Plant Biol. 2014, 56, 1064–1079. [Google Scholar] [CrossRef]
  77. van Buer, J.; Cvetkovic, J.; Baier, M. Cold Regulation of Plastid Ascorbate Peroxidases Serves as A Priming Hub Controlling ROS Signaling in Arabidopsis thaliana. BMC Plant Biol. 2016, 16, 163. [Google Scholar] [CrossRef] [Green Version]
  78. Zhao, H.; Ye, L.; Wang, Y.; Zhou, X.; Yang, J.; Wang, J.; Cao, K.; Zou, Z. Melatonin Increases the Chilling Tolerance of Chloroplast in Cucumber Seedlings by Regulating Photosynthetic Electron Flux and the Ascorbate-Glutathione Cycle. Front. Plant Sci. 2016, 7, 1814. [Google Scholar] [CrossRef] [Green Version]
  79. Soliman, M.H.; Alayafi, A.A.M.; El Kelish, A.A.; Abu-Elsaoud, A.M. Acetylsalicylic Acid Enhance Tolerance of Phaseolus vulgaris L. to Chilling Stress, Improving Photosynthesis, Antioxidants and Expression of Cold Stress Responsive Genes. Bot. Stud. 2018, 59, 6. [Google Scholar] [CrossRef] [Green Version]
  80. Wang, S.; Bai, G.; Wang, S.; Yang, L.; Yang, F.; Wang, Y.; Zhu, J.K.; Hua, J. Chloroplast RNA-Binding Protein RBD1 Promotes Chilling Tolerance through 23S rRNA Processing in Arabidopsis. PLoS Genet. 2016, 12, e1006027. [Google Scholar] [CrossRef]
  81. He, Y.; Yu, C.; Zhou, L.; Chen, Y.; Liu, A.; Jin, J.; Hong, J.; Qi, Y.; Jiang, D. Rubisco Decrease is Involved in Chloroplast Protrusion and Rubisco-containing Body Formation in Soybean (Glycine max.) Under Salt Stress. Plant Physiol. Biochem. 2014, 74, 118–124. [Google Scholar] [CrossRef]
  82. Hossain, M.S.; ElSayed, A.I.; Moore, M.; Dietz, K.J. Redox and Reactive Oxygen Species Network in Acclimation for Salinity Tolerance in Sugar Beet. J. Exp. Bot. 2017, 68, 1283–1298. [Google Scholar] [CrossRef] [Green Version]
  83. Ling, Q.; Jarvis, P. Regulation of Chloroplast Protein Import by the Ubiquitin E3 Ligase SP1 Is Important for Stress Tolerance in Plants. Curr. Biol. 2015, 25, 2527–2534. [Google Scholar] [CrossRef] [Green Version]
  84. Ling, Q.; Jarvis, P. Plant Signaling: Ubiquitin Pulls the Trigger on Chloroplast Degradation. Curr. Biol. 2016, 26, R38–R40. [Google Scholar] [CrossRef] [Green Version]
  85. Pulido, P.; Llamas, E.; Rodriguez-Concepcion, M. Both Hsp70 Chaperone and Clp Protease Plastidial Systems are Required for Protection Against Oxidative Stress. Plant Signal Behav. 2017, 12, e1290039. [Google Scholar] [CrossRef] [Green Version]
  86. Nawaz, G.; Lee, K.; Park, S.J.; Kim, Y.O.; Kang, H. A Chloroplast-Targeted Cabbage DEAD-box RNA Helicase BrRH22 Confers Abiotic Stress Tolerance to Transgenic Arabidopsis Plants by Affecting Translation of Chloroplast Transcripts. Plant Physiol. Biochem. 2018, 127, 336–342. [Google Scholar] [CrossRef]
  87. Guddimalli, R.; Somanaboina, A.K.; Palle, S.R.; Edupuganti, S.; Kummari, D.; Palakolanu, S.R.; Naravula, J.; Gandra, J.; Qureshi, I.A.; Marka, N.; et al. Overexpression of RNA-binding Bacterial Chaperones in Rice Leads to Stay-green Phenotype, Improved Yield and Tolerance to Salt and Drought Stresses. Physiol. Plant. 2021, 173, 1351–1368. [Google Scholar] [CrossRef]
  88. Schuster, M.; Gao, Y.; Schöttler, M.A.; Bock, R.; Zoschke, R. Limited Responsiveness of Chloroplast Gene Expression during Acclimation to High Light in Tobacco. Plant Physiol. 2020, 182, 424–435. [Google Scholar] [CrossRef] [Green Version]
  89. Sun, Y.; Gao, Y.; Wang, H.; Yang, X.; Zhai, H.; Du, Y. Stimulation of Cyclic Electron Flow around PSI As a Response to the Combined Stress of High Light and High Temperature in Grape Leaves. Funct. Plant Biol. 2018, 45, 1038–1045. [Google Scholar] [CrossRef]
  90. Exposito-Rodriguez, M.; Laissue, P.P.; Yvon-Durocher, G.; Smirnoff, N.; Mullineaux, P.M. Photosynthesis-Dependent H2O2 Transfer from Chloroplasts to Nuclei Provides a High-light Signalling Mechanism. Nat. Commun. 2017, 8, 49. [Google Scholar] [CrossRef] [Green Version]
  91. Malnoë, A.; Wang, F.; Girard-Bascou, J.; Wollman, F.A.; de Vitry, C. Thylakoid FtsH Protease Contributes to Photosystem II and Cytochrome B6f Remodeling in Chlamydomonas reinhardtii under Stress Conditions. Plant Cell 2014, 26, 373–390. [Google Scholar] [CrossRef] [Green Version]
  92. Miller, G.; Suzuki, N.; Ciftci-Yilmaz, S.; Mittler, R. Reactive Oxygen Species Homeostasis and Signalling During Drought and Salinity Stresses. Plant Cell Environ. 2010, 33, 453–467. [Google Scholar] [CrossRef]
  93. Lim, S.D.; Lee, C.; Jang, C.S. The Rice RING E3 ligase, OsCTR1, Inhibits Trafficking to The Chloroplasts of OsCP12 and OsRP1, and Its Overexpression Confers Drought Tolerance in Arabidopsis. Plant Cell Environ. 2014, 37, 1097–1113. [Google Scholar] [CrossRef]
  94. Yoo, Y.H.; Nalini Chandran, A.K.; Park, J.C.; Gho, Y.S.; Lee, S.W.; An, G.; Jung, K.H. OsPhyB-Mediating Novel Regulatory Pathway for Drought Tolerance in Rice Root Identified by a Global RNA-Seq Transcriptome Analysis of Rice Genes in Response to Water Deficiencies. Front. Plant Sci. 2017, 8, 580. [Google Scholar] [CrossRef]
  95. Abbaraju, H.K.R.; Gupta, R.; Appenzeller, L.M.; Fallis, L.P.; Hazebroek, J.; Zhu, G.; Bourett, T.M.; Howard, R.J.; Weers, B.; Lafitte, R.H.; et al. A vegetative storage protein improves drought tolerance in maize. Plant Biotechnol. J. 2021. [Google Scholar] [CrossRef]
  96. Wen, Z.; Wang, Y.; Xia, C.; Zhang, Y.; Zhang, H. Chloroplastic SaNADP-ME4 of C(3)-C(4) Woody Desert Species Salsola laricifolia Confers Drought and Salt Stress Resistance to Arabidopsis. Plants 2021, 10, 1827. [Google Scholar] [CrossRef] [PubMed]
  97. Gómez-Ocampo, G.; Ploschuk, E.L.; Mantese, A.; Crocco, C.D.; Botto, J.F. BBX21 Reduces Abscisic Acid Sensitivity, Mesophyll Conductance and Chloroplast Electron Transport Capacity to Increase Photosynthesis and Water Use Efficiency in Potato Plants Cultivated Under Moderated Drought. Plant J. 2021, 108, 1131–1144. [Google Scholar] [CrossRef]
  98. Faye, J.M.; Akata, E.A.; Sine, B.; Diatta, C.; Cisse, N.; Fonceka, D.; Morris, G.P. Quantitative and Population Genomics Suggest a Broad Role of Stay-Green Loci In the Drought Adaptation of Sorghum. Plant Genome 2021, e20176. [Google Scholar] [CrossRef]
  99. Park, E.; Nedo, A.; Caplan, J.L.; Dinesh-Kumar, S.P. Plant-Microbe Interactions: Organelles and the Cytoskeleton in Action. New Phytol. 2018, 217, 1012–1028. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  100. Nomura, H.; Komori, T.; Uemura, S.; Kanda, Y.; Shimotani, K.; Nakai, K.; Furuichi, T.; Takebayashi, K.; Sugimoto, T.; Sano, S.; et al. Chloroplast-Mediated Activation of Plant Immune Signalling in Arabidopsis. Nat. Commun. 2012, 3, 926. [Google Scholar] [CrossRef] [Green Version]
  101. de Torres Zabala, M.; Littlejohn, G.; Jayaraman, S.; Studholme, D.; Bailey, T.; Lawson, T.; Tillich, M.; Licht, D.; Bölter, B.; Delfino, L.; et al. Chloroplasts Play a Central Role in Plant Defence and Are Targeted by Pathogen Effectors. Nat. Plants 2015, 1, 15074. [Google Scholar] [CrossRef]
  102. Bilgin, D.D.; Zavala, J.A.; Zhu, J.; Clough, S.J.; Ort, D.R.; DeLucia, E.H. Biotic Stress Globally Downregulates Photosynthesis Genes. Plant Cell Environ. 2010, 33, 1597–1613. [Google Scholar] [CrossRef] [Green Version]
  103. Göhre, V.; Jones, A.M.; Sklenář, J.; Robatzek, S.; Weber, A.P. Molecular Crosstalk between PAMP-triggered Immunity and Photosynthesis. Mol. Plant Microbe Interact. 2012, 25, 1083–1092. [Google Scholar] [CrossRef]
  104. Caplan, J.L.; Kumar, A.S.; Park, E.; Padmanabhan, M.S.; Hoban, K.; Modla, S.; Czymmek, K.; Dinesh-Kumar, S.P. Chloroplast Stromules Function during Innate Immunity. Dev. Cell 2015, 34, 45–57. [Google Scholar] [CrossRef] [Green Version]
  105. Park, E.; Caplan, J.L.; Dinesh-Kumar, S.P. Dynamic Coordination of Plastid Morphological Change by Cytoskeleton for Chloroplast-Nucleus Communication during Plant Immune Responses. Plant Signal Behav. 2018, 13, e1500064. [Google Scholar] [CrossRef] [Green Version]
  106. Ding, X.; Jimenez-Gongora, T.; Krenz, B.; Lozano-Duran, R. Chloroplast Clustering around the Nucleus is A General Response to Pathogen Perception in Nicotiana benthamiana. Mol. Plant Pathol. 2019, 20, 1298–1306. [Google Scholar] [CrossRef] [Green Version]
  107. Akimoto-Tomiyama, C.; Tanabe, S.; Kajiwara, H.; Minami, E.; Ochiai, H. Loss of Chloroplast-Localized Protein Phosphatase 2Cs in Arabidopsis thaliana Leads to Enhancement of Plant Immunity and Resistance to Xanthomonas campestris pv. campestris Infection. Mol. Plant Pathol. 2018, 19, 1184–1195. [Google Scholar] [CrossRef] [Green Version]
  108. Erickson, J.L.; Adlung, N.; Lampe, C.; Bonas, U.; Schattat, M.H. The Xanthomonas effector XopL Uncovers the Role of Microtubules in Stromule Extension and Dynamics in Nicotiana benthamiana. Plant J. 2018, 93, 856–870. [Google Scholar] [CrossRef] [Green Version]
  109. Gou, J.Y.; Li, K.; Wu, K.; Wang, X.; Lin, H.; Cantu, D.; Uauy, C.; Dobon-Alonso, A.; Midorikawa, T.; Inoue, K.; et al. Wheat Stripe Rust Resistance Protein WKS1 Reduces the Ability of the Thylakoid-Associated Ascorbate Peroxidase to Detoxify Reactive Oxygen Species. Plant Cell 2015, 27, 1755–1770. [Google Scholar] [CrossRef]
  110. Wang, S.; Li, Q.P.; Wang, J.; Yan, Y.; Zhang, G.L.; Yan, Y.; Zhang, H.; Wu, J.; Chen, F.; Wang, X.; et al. YR36/WKS1-Mediated Phosphorylation of PsbO, an Extrinsic Member of Photosystem II, Inhibits Photosynthesis and Confers Stripe Rust Resistance in Wheat. Mol. Plant 2019, 12, 1639–1650. [Google Scholar] [CrossRef] [Green Version]
  111. Hamel, L.P.; Sekine, K.T.; Wallon, T.; Sugiwaka, Y.; Kobayashi, K.; Moffett, P. The Chloroplastic Protein THF1 Interacts with the Coiled-Coil Domain of the Disease Resistance Protein N’ and Regulates Light-Dependent Cell Death. Plant Physiol. 2016, 171, 658–674. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  112. Jiang, G.; Yin, D.; Zhao, J.; Chen, H.; Guo, L.; Zhu, L.; Zhai, W. The Rice Thylakoid Membrane-Bound Ascorbate Peroxidase OsAPX8 Functions in Tolerance to Bacterial Blight. Sci. Rep. 2016, 6, 26104. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  113. Liu, M.; Zhang, S.; Hu, J.; Sun, W.; Padilla, J.; He, Y.; Li, Y.; Yin, Z.; Liu, X.; Wang, W.; et al. Phosphorylation-Guarded Light-Harvesting complex II Contributes to Broad-Spectrum Blast Resistance in Rice. Proc. Natl. Acad. Sci. USA 2019, 116, 17572–17577. [Google Scholar] [CrossRef] [Green Version]
  114. Ishiga, Y.; Ishiga, T.; Ikeda, Y.; Matsuura, T.; Mysore, K.S. NADPH-Dependent Thioredoxin Reductase C Plays a Role in Nonhost Disease Resistance Against Pseudomonas syringae Pathogens by Regulating Chloroplast-Generated Reactive Oxygen Species. Peer. J. 2016, 4, e1938. [Google Scholar] [CrossRef] [Green Version]
  115. Su, J.; Yang, L.; Zhu, Q.; Wu, H.; He, Y.; Liu, Y.; Xu, J.; Jiang, D.; Zhang, S. Active Photosynthetic Inhibition Mediated by MPK3/MPK6 is Critical to Effector-Triggered Immunity. PLoS Biol. 2018, 16, e2004122. [Google Scholar] [CrossRef]
  116. Lewis, L.A.; Polanski, K.; de Torres-Zabala, M.; Jayaraman, S.; Bowden, L.; Moore, J.; Penfold, C.A.; Jenkins, D.J.; Hill, C.; Baxter, L.; et al. Transcriptional Dynamics Driving MAMP-Triggered Immunity and Pathogen Effector-Mediated Immunosuppression in Arabidopsis Leaves Following Infection with Pseudomonas syringae pv tomato DC3000. Plant Cell 2015, 27, 3038–3064. [Google Scholar] [CrossRef] [Green Version]
  117. Li, G.; Froehlich, J.E.; Elowsky, C.; Msanne, J.; Ostosh, A.C.; Zhang, C.; Awada, T.; Alfano, J.R. Distinct Pseudomonas Type-III Effectors Use a Cleavable Transit Peptide to Target Chloroplasts. Plant J. 2014, 77, 310–321. [Google Scholar] [CrossRef]
  118. Rodríguez-Herva, J.J.; González-Melendi, P.; Cuartas-Lanza, R.; Antúnez-Lamas, M.; Río-Alvarez, I.; Li, Z.; López-Torrejón, G.; Díaz, I.; Del Pozo, J.C.; Chakravarthy, S.; et al. A Bacterial Cysteine Protease Effector Protein Interferes with Photosynthesis to Suppress Plant Innate Immune Responses. Cell Microbiol. 2012, 14, 669–681. [Google Scholar] [CrossRef] [Green Version]
  119. Wangdi, T.; Uppalapati, S.R.; Nagaraj, S.; Ryu, C.M.; Bender, C.L.; Mysore, K.S. A Virus-Induced Gene Silencing Screen Identifies a Role for Thylakoid Formation1 in Pseudomonas syringae pv Tomato Symptom Development in Tomato and Arabidopsis. Plant Physiol. 2010, 152, 281–292. [Google Scholar] [CrossRef] [Green Version]
  120. Rossi, F.R.; Krapp, A.R.; Bisaro, F.; Maiale, S.J.; Pieckenstain, F.L.; Carrillo, N. Reactive Oxygen Species Generated in Chloroplasts Contribute to Tobacco Leaf Infection by the Necrotrophic Fungus Botrytis cinerea. Plant J. 2017, 92, 761–773. [Google Scholar] [CrossRef] [Green Version]
  121. Nakano, M.; Mukaihara, T. Ralstonia solanacearum Type III Effector RipAL Targets Chloroplasts and Induces Jasmonic Acid Production to Suppress Salicylic Acid-Mediated Defense Responses in Plants. Plant Cell Physiol. 2018, 59, 2576–2589. [Google Scholar] [CrossRef] [PubMed]
  122. Faris, J.D.; Zhang, Z.; Lu, H.; Lu, S.; Reddy, L.; Cloutier, S.; Fellers, J.P.; Meinhardt, S.W.; Rasmussen, J.B.; Xu, S.S.; et al. A Unique Wheat Disease Resistance-like Gene Governs Effector-triggered Susceptibility to Necrotrophic Pathogens. Proc. Natl. Acad. Sci. USA 2010, 107, 13544–13549. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  123. Gao, C.; Xu, H.; Huang, J.; Sun, B.; Zhang, F.; Savage, Z.; Duggan, C.; Yan, T.; Wu, C.H.; Wang, Y.; et al. Pathogen Manipulation of Chloroplast Function Triggers a Light-dependent Immune Recognition. Proc. Natl. Acad. Sci. USA 2020, 117, 9613–9620. [Google Scholar] [CrossRef] [Green Version]
  124. Tang, L.; Yang, G.; Ma, M.; Liu, X.; Li, B.; Xie, J.; Fu, Y.; Chen, T.; Yu, Y.; Chen, W.; et al. An Effector of a Mecrotrophic Fungal Pathogen Targets the Calcium-sensing Receptor in Chloroplasts to Inhibit Host Resistance. Mol. Plant Pathol. 2020, 21, 686–701. [Google Scholar] [CrossRef] [PubMed] [Green Version]
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Figure 1. An overview of the various mechanisms in chloroplast response to adverse stresses. Adverse environmental stresses cause perturbations and generate signals in chloroplasts that regulate chloroplast gene expression and protein remodeling. A series of cellular activities are then triggered to restore chloroplast homeostasis. Adverse conditions can affect the structure, function, and development of chloroplasts. Chloroplasts synthesize biologically active compounds and phytohormones to acclimate to stresses. Moreover, the chloroplast is able to communicate its status to the nucleus through retrograde signaling to regulate nuclear stress-responsive genes. The SAL1/PAP, MEcPP, and ROS pathways act as important components of the chloroplast retrograde signaling pathway. Dashed lines indicate postulated regulation. ROS, reactive oxygen species; EX1/2, executor 1/2; MEcPP, methylerythritol cyclodiphosphate; PAP, phosphonucleotide 3′-phosphoadenosine 5′-phosphate.
Figure 1. An overview of the various mechanisms in chloroplast response to adverse stresses. Adverse environmental stresses cause perturbations and generate signals in chloroplasts that regulate chloroplast gene expression and protein remodeling. A series of cellular activities are then triggered to restore chloroplast homeostasis. Adverse conditions can affect the structure, function, and development of chloroplasts. Chloroplasts synthesize biologically active compounds and phytohormones to acclimate to stresses. Moreover, the chloroplast is able to communicate its status to the nucleus through retrograde signaling to regulate nuclear stress-responsive genes. The SAL1/PAP, MEcPP, and ROS pathways act as important components of the chloroplast retrograde signaling pathway. Dashed lines indicate postulated regulation. ROS, reactive oxygen species; EX1/2, executor 1/2; MEcPP, methylerythritol cyclodiphosphate; PAP, phosphonucleotide 3′-phosphoadenosine 5′-phosphate.
Ijms 22 13464 g001
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Song, Y.; Feng, L.; Alyafei, M.A.M.; Jaleel, A.; Ren, M. Function of Chloroplasts in Plant Stress Responses. Int. J. Mol. Sci. 2021, 22, 13464. https://doi.org/10.3390/ijms222413464

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Song Y, Feng L, Alyafei MAM, Jaleel A, Ren M. Function of Chloroplasts in Plant Stress Responses. International Journal of Molecular Sciences. 2021; 22(24):13464. https://doi.org/10.3390/ijms222413464

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Song, Yun, Li Feng, Mohammed Abdul Muhsen Alyafei, Abdul Jaleel, and Maozhi Ren. 2021. "Function of Chloroplasts in Plant Stress Responses" International Journal of Molecular Sciences 22, no. 24: 13464. https://doi.org/10.3390/ijms222413464

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