three-dimensional analysis of chloroplast …...35 y.z.), the research grants council of hong kong...

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Three-dimensional analysis of chloroplast structures associated with virus 1

infection 2

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Xuejiao Jin, Zhihao Jiang, Kun Zhang, Pengfei Wang, Xiuling Cao, Ning Yue, 4

Xueting Wang, Xuan Zhang, Yunqin Li, Dawei Li, Byung-Ho Kang, and Yongliang 5

Zhang* 6

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State Key Laboratory of Agro-Biotechnology and Ministry of Agriculture Key 8

Laboratory of Soil Microbiology, College of Biological Sciences, China Agricultural 9

University, Beijing 100193, P. R. China (X.J., Z.J., K.Z., X.C., N.Y., X.W., X.Z., D.L., 10

Y.Z.); School of Life Sciences, Center for Cell and Developmental Biology and State 11

Key Laboratory of Agro-biotechnology, The Chinese University of Hong Kong, Hong 12

Kong, P. R. China (P.W., B-H.K.); Institute of Biotechnology, Zhejiang University, 13

Hangzhou, P. R. China (Y.L.) 14

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* Corresponding authors: Yongliang Zhang, Ph. D and Associate Professor, China 16

Agricultural University 17

Phone: +86-10-62733190, Fax: +86-10-62732012, E-mail: [email protected] 18

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Running Title: 3D architecture of chloroplast during viral attack. 20

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One sentence summary: Three-dimensional visualization identifies structural 22 remodelling in chloroplasts during barley stripe mosaic virus infection 23

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Author contributions: Y.Z., X.J., K.Z., and D.L. conceived and designed the study. 26

X.J., Y.Z., Z.J., K.Z., P.W., X.C., N.Y., X.W., X.Z., and Y.L. performed the 27

experiments. Y.Z., X.J., K.Z., P.W., D.L., and B-H.K. analyzed the data. X.J., Y.Z., 28

B-H.K., and D.L. wrote the article. 29

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Plant Physiology Preview. Published on August 18, 2017, as DOI:10.1104/pp.17.00871

Copyright 2017 by the American Society of Plant Biologists

www.plantphysiol.orgon February 11, 2020 - Published by Downloaded from Copyright © 2017 American Society of Plant Biologists. All rights reserved.

http://www.plantphysiol.org

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Funding information: This work was supported by the National Natural Science 31

Foundation of China (grant nos. 31570143 and 31270184 to D.L.), the Project for 32

Extramural Scientists of SKLAB (grant no. 2017SKLAB1-6 to D.L. and B-H.K.), the 33

Fundamental Research Funds for the Central Universities (grant no. 2017SY003 to 34

Y.Z.), the Research Grants Council of Hong Kong (grant nos. GRF14126116, 35

AoE/M-05/12, C4011-14R to B-H.K.), and the Cooperative Research Program for 36

Agriculture Science and Technology Development of the Rural Development 37

Administration, Republic of Korea (grant no. PJ010953092015 to B-H.K.). 38

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Abstract 40

Chloroplasts are multifunctional organelles whose morphology is affected by 41

environmental stresses. Although the three-dimensional (3D) architecture of thylakoid 42

membranes has been reported previously, a 3D visualization of chloroplast under 43

stress has not been explored. In this work, we used a positive-strand RNA [(+)RNA] 44

virus, Barley stripe mosaic virus (BSMV) to observe chloroplast structural changes 45

during infection by electron tomography (ET). The analyses revealed remodeling of 46

the chloroplast membranes, characterized by the clustering of outer 47

membrane-invaginated spherules in inner membrane-derived packets. Diverse 48

morphologies of cytoplasmic invaginations (CIs) were evident with spherules at the 49

periphery and different sized openings connecting the CIs to the cytoplasm. 50

Immunoelectron microscopy of these viral components verified that the aberrant 51

membrane structures were sites for BSMV replication. The BSMV αa replication 52

protein localized at the surface of the chloroplasts and played a prominent role in 53

eliciting chloroplast membrane rearrangements. In sum, our results have revealed the 54

3D structure of the chloroplasts induced by BSMV infection. These findings 55

contribute to our understanding of chloroplast morphological changes under stress 56

conditions, and during assembly of plant (+)RNA virus replication complexes. 57

58

59



4

Chloroplasts are responsible for the eukaryotic photosynthesis and carbon fixation, 60

thus providing energy for much of life on the earth. Chloroplast biogenesis is a 61

complex process and is highly integrated with cellular and plant development (Yang 62

et al., 2010; Pogson et al., 2015). Although 3D models of the thylakoid membrane 63

architecture have been created using electron tomography (ET) of higher plant 64

chloroplasts (Shimoni et al., 2005; Daum et al., 2010; Austin and Staehelin, 2011; 65

Kowalewska et al., 2016) and Chlamydomonas reinhardtii chloroplasts (Engel et al., 66

2015), a 3D visualization of chloroplasts changes in response to external stresses (eg. 67

viral attack) have not been investigated. 68

Positive-strand RNA viruses often manipulate host membrane systems to form 69

microenvironments for replication and use diverse intracellular membranes to 70

assemble viral replication complexes (VRCs) (Salonen et al., 2005; Laliberte and 71

Sanfacon, 2010; Verchot, 2011; Romero-Brey and Bartenschlager, 2014). The VRCs, 72

on one hand, are thought to shield viruses from host defense systems such as RNA 73

silencing, and on the other hand, provide a microenvironment for enriching viral 74

replication proteins, diverse host factors and energy needed for efficient replication of 75

progeny viral RNAs (Schwartz et al., 2004; Novoa et al., 2005; Miller and 76

Krijnse-Locker, 2008; Verchot, 2011). VRCs have been detected in mitochondrial 77

membranes (Kopek et al., 2007), endoplasmic reticulum membranes 78

(Reatrepo-Hartwig and Ahlquis, 1996), chloroplast membranes (Hatta et al., 1973), 79

and peroxisomal membranes (de Castro et al., 2017). Intriguingly, some viruses, such 80

as Tomato bushy stunt virus (TBSV), can utilize alternative organelles for replication 81

(Jonczyk et al., 2007; Xu and Nagy, 2014). Despite the different locations of VRCs, 82

the viral replication compartments share some common features such as invaginated 83

vesicles/spherules or double membrane vesicle (DMV) structures, and a pore-like 84

opening to the cytoplasm (Boon et al., 2010; Paul and Bartenschlager, 2013). 85

Random sectioning used in conventional electron microscopy often misses crucial and 86

subtle structural dimensions such as the sizes and shapes of vesicles (Baumeister, 87

2002). To more fully understand membrane structures within organelles and their 88

functions, electron tomography (ET) based on transmission electron microscopy 89



5

(TEM) or dual beam focused ion beam scanning electron microscopy (FIB-SEM) are 90

increasingly used for three-dimensional (3D) reconstructions of altered membranes 91

during viral infection (Laliberte and Zheng, 2014; Risco et al., 2014; Harak and 92

Lohmann, 2015; Fernandez de Castro et al., 2017). Kopek et al. reported the first 3D 93

architecture of the membrane-bound (+)RNA virus replication compartments in Flock 94

House virus (FHV)-infected Drosophila cells (Kopek et al., 2007). A recent electron 95

tomographic analysis of Turnip mosaic virus (TuMV)-induced intracellular 96

rearrangements revealed that the vesicle-like structures apparent in two-dimensional 97

(2D) TEM images are, in fact, tubules (Wan et al., 2015). In 2015, a reconstruction 98

analysis of ER-derived membranous spherules induced during Beet black scorch virus 99

(BBSV) infection provided the first 3D model of VRCs of a plant (+)RNA virus (Cao 100

et al., 2015). Gomez-Aix et al. also determined the 3D architecture of remodeled 101

mitochondria in Melon necrotic spot virus-infected cells by focused ion beam-field 102

emission scanning electron microscopy (FIB-FESEM) (Gomez-Aix et al., 2015). 103

Collectively, electron tomography has become a powerful tool that can accurately 104

define the overall architecture of intracellular membranes as well as changes in 105

organelles during virus infection. 106

Viral proteins often play crucial roles in mediating the rearrangement of host 107

endomembrane systems during virus infection (Paul and Bartenschlager, 2013). For 108

example, Hepatitis C virus (HCV) NS5A and NS4B can induce the formation of 109

double and single membrane vesicles, respectively (Romero-Brey et al., 2012). Brome 110

mosaic virus (BMV) expression of different ratios of the 1a and 2a proteins induces 111

distinct spherules with altered sizes (Schwartz et al., 2004). The Closterovirus 1a and 112

1ab proteins also facilitate membrane remodeling and formation of multivesicular 113

replication platforms (Gushchin et al., 2017). TuMV 6K2 is responsible for 114

endomembrane alterations (Beauchemin et al., 2007). In addition, it has also become 115

evident that remodeling of host endomembrane systems involves participation of viral 116

RNAs and diverse host factors (Kallio et al., 2013; Wang, 2015; Kovalev et al., 2016). 117

Barley stripe mosaic virus (BSMV) is the type member of the genus Hordeivirus and 118

infects numerous monocots and dicots (Jackson et al., 2009). BSMV has a tripartite 119



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positive-strand RNA genome encoding seven major proteins. The αa and γa proteins 120

are encoded by the RNAα and RNAγ genomes, respectively, and are essential for 121

BSMV RNA replication. RNAβ encodes the coat protein (CP) for viral RNA 122

encapsidation, and subgenomic (sg) RNAs derived from RNAβ serve as mRNAs for 123

the triple gene block (TGB) proteins responsible for cell-to-cell movement. The 124

multifunctional γb protein is a BSMV pathogenicity determinant that is translated 125

from sgRNAγ (Jackson et al., 2009). During BSMV infection and VRC formation, 126

chloroplast abnormalities are induced that include cytoplasmic invaginations (CIs), 127

and peripheral vesicles in the chloroplasts (Carroll, 1970; McMullen et al., 1978; Lin 128

and Langenberg, 1984, 1985; Torrance et al., 2006). Although previous studies 129

indicated that chloroplasts are deformed in BSMV-infected plant cells, aberrant 130

chloroplast structures arising during infection, particularly the 3D architecture and the 131

molecular mechanisms underlying formation of the chloroplast-derived membranous 132

structures have not been investigated in detail. To clarify details of the chloroplast 133

architecture in BSMV-infected Nicotiana benthamiana, we performed electron 134

tomography to unravel the 3D structure of abnormal chloroplast-derived VRCs and 135

CIs, and carried out experiments to explore the functions of viral factors functioning 136

in remodeling the chloroplasts. 137

138

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RESULTS 140

Ultrastructural Analysis of BSMV-Infected Cells by Transmission Electron 141

Microscopy 142

To investigate the ultrastructural changes in cells during BSMV infection, leaf tissues 143

from healthy or BSMV-infected Nicotiana benthamiana leaves were chemically fixed 144

and embedded in resin for transmission electron microscopic analysis. During BSMV 145

infection, dramatic alterations of chloroplast structure occurred as CIs containing 146

large amounts of virus-like particles, and peripheral invaginations appeared (Fig. 1, 147

B-D), whereas similar structures were absent in uninfected N. benthamiana 148

chloroplasts (Fig. 1A). Interestingly, membrane invaginations connected to CIs were 149

also observed at the periphery of the CIs (Fig. 1C, white arrows), and they were very 150

similar to the other invaginations at the chloroplast periphery (Fig. 1, C and D, white 151

arrowheads). In addition, spherules with an ~50 nm diameter were observed 152

occasionally within chloroplast envelope invaginations (Fig. 1D, boxed region). 153

Moreover, other cellular changes including membrane inclusions and elongated 154

mitochondria were observed occasionally (Supplemental Fig. S1, A and B). At the late 155

stages of BSMV infection, cytoplasm containing large amounts of virus-like particles 156

often protruded into the vacuole (Supplemental Fig. S1C). Taken together, these 157

results reveal that numerous dramatic cytopathological changes are induced during 158

BSMV infection, in particular chloroplasts membrane remodeling. 159

160

Localization of BSMV Double-Stranded RNAs (dsRNA) and Proteins in 161

BSMV-induced Chloroplast Membrane Structures 162

Our previous results revealed that chloroplasts are sites for replication of BSMV 163

(Zhang et al., 2017). To further determine whether the BSMV replication protein αa, 164

and dsRNA replicative intermediates associate with chloroplast-derived membrane 165

structures, immunoelectron microscopy (IEM) was performed. Gold particles 166

conjugated to dsRNA antibodies specifically labeled chloroplast invaginations of the 167

chloroplast envelope or at the periphery of the CIs (Fig. 2, A and B, boxed regions). 168

Meanwhile, antibodies against the αa protein showed specific labeling of the 169



8

chloroplasts, which was characterized by the distribution of gold particles on the 170

envelope membranes, invaginations, and the CI membranes (Fig. 2, C-E, boxed 171

regions and arrowheads). In addition, labeling with a BSMV CP-specific antiserum 172

revealed specific decoration of virus-like particles within the CIs, as well as the 173

cytoplasm (Fig. 2, F and G), demonstrating that the abundant virus-like particles 174

present within the CIs are indeed the BSMV virions. For control healthy leaf tissue, 175



9

only a very low background labeling was detected in the chloroplasts or other cellular 176

regions (Supplemental Fig. S2). 177

Moreover, chloroplasts from mock- and BSMV-inoculated N. benthamiana leaves 178

were purified, and subjected to Western blot and RT-PCR analyses (Supplemental Fig. 179

S3). The results showed that the αa protein and the CP can be readily detected in 180

chloroplasts purified from the BSMV-infected leaf tissues, but not from 181



10

mock-inoculated plants (Supplemental Fig. S3A). As a control, potential 182

contamination of the purified chloroplasts by cytoplasmic constituents was eliminated 183

because the cytoplasmic-localized PEPC was only detected in total protein extracts 184

from leaf tissues, but not from isolated chloroplasts (Supplemental Fig. S3A). 185

RT-PCR analysis also showed that both plus- and minus-strand BSMV RNAs were 186

present in the isolated chloroplasts. Controls also indicated that chloroplast PSII core 187

protein C (psbC) was restricted to the chloroplast fraction, whereas cytoplasmic 18S 188

ribosomal RNA (18S rRNA) control was difficult to detect in the isolated chloroplasts 189

(Supplemental Fig. S3B). Collectively, these data indicate that viral RNA synthesis 190

occurs in the chloroplast membrane invaginations. 191

192

Three-Dimensional (3D) Reconstruction of BSMV-Induced Chloroplast 193

Membrane Structures 194

To characterize the 3D architecture of BSMV replication factories, and the CIs of 195

chloroplasts induced by BSMV, we performed electron tomography analysis. The 196

results showed that peripheral invaginations and spherules from the envelope 197

membranes and large CIs are present in the remodeled chloroplasts (Fig. 3A), whereas 198

such structural abnormalities in chloroplasts were absent in healthy N. benthamiana 199

cells (Supplemental Movie S1). The peripheral invaginations were continuous with 200

the inner chloroplast membrane, but not the outer membrane (Fig. 3, B and C, 201

arrowheads), and spherules were frequently observed inside the inner 202

membrane-invaginated packets (Fig. 3, B and C; Supplemental Movie S2). These 203

spherules were connected to the outer membrane in some slices (Fig. 3, B and C), 204

indicating that the smaller spherules are invaginations of the outer membrane. In 205

addition, one or more spherules were surrounded by inner membrane-derived packets 206

(Fig. 3, B and C; Supplemental Movie S2), and the CIs with large amounts of virus 207

particles inside were double-membrane bounded (Fig. 3A; Supplemental Fig. S4, A 208

and B). A 3D surface rendering of the chloroplast membranes clearly demonstrates 209

that all of the spherules (Fig. 3D, light yellow) originate from the outer membranes 210

(Fig. 3D, light blue) and have a tight neck-like opening to the cytoplasm (Fig. 3H, 211



11

arrowhead and black dashed circle). The inner chloroplast membrane-derived 212

invaginations (Fig. 3, D, E and G, translucent white) form packets of varying sizes 213

that enclose one or more outer membrane-derived spherules (Fig. 3, D-G; 214

Supplemental Movies S3-S4). The inner membrane invaginations had an average 215

diameter of 112 ± 41 nm (n = 16). The average length and width of the spherules were 216

55 ± 8 nm and 42 ± 7 nm (n = 20), respectively, and their necks had an average 217



12

diameter of 11 ± 4 nm (n = 20). Taken together, 3D electron tomography clearly 218

revealed that the chloroplast invaginations are composed of inner chloroplast 219

membrane-derived packets containing variable numbers of outer membrane-derived 220

spherules. Each of the spherules has a narrow opening to the cytoplasm, supporting a 221

role in BSMV replication. 222

223

FIB-SEM Tomography of the Chloroplasts Reveals Diverse Morphology of CIs 224

During BSMV Infection 225

In addition to peripheral invaginations on the chloroplast surfaces (Fig. 3D), another 226

remarkable feature of BSMV-induced chloroplast abnormalities is the formation of 227

CIs (Fig. 1 and Fig. 3). Electron tomography was also performed to characterize the 228

CIs. Transmission electron tomographic analyses revealed that CIs are bound by 229

double membranes and that some invaginations are present at the periphery of the CIs 230

(Supplemental Fig. S4, A and B). Furthermore, spherules were also observed in these 231

invaginations and were connected to the CI (Supplemental Fig. S4B, arrowheads), 232

and are similar to spherules within the chloroplast membrane packets as described in 233

Figure 3B. A 3D surface rendering of the CI confirmed that these spherules are 234

identical to the chloroplast outer membrane-invaginated spherules, as evidenced by 235

their similar sizes and external connections (Supplemental Fig. S4, C-F; Fig. 3D; 236

Supplemental Movies S4-S5). Due to the large sizes of the CIs, we could only obtain 237

partial CI structures by transmission electron tomography (Supplemental Fig. S4, C 238

and D; Supplemental Movie S5). Nevertheless, these preliminary data imply that the 239

CIs resemble cavern-like structures generated by continuous invagination of the 240

chloroplast envelope membranes. 241

In order to reconstruct whole chloroplast CI structures, FIB-SEM, a powerful tool to 242

determine the structures of large organelles, was performed to reconstruct the whole 243

chloroplast with CIs. Figure 4A-D shows different slices from the same chloroplast. 244

The images clearly show that a small CI opening was present in some slices (Fig. 4, B 245

and C, arrowheads), but that the openings were not evident in contiguous slices (Fig. 246

4, A and D, arrowheads). These results indicate that the above CI has a very small 247



13

opening because the distance between the two slices is only 50 nm. In addition, a 248

mitochondrion was enclosed in the CI of this chloroplast (Fig. 4, A-D). However, in 249

some chloroplasts, the opening of the CI is very large (Fig. 4, E-H, arrowheads). A 3D 250

reconstruction of the chloroplast shown in Figure 4A-D reveals a large number of 251

small invaginations (Fig. 4, I and J, white arrowheads) at the surface of the 252

chloroplast (Fig. 4, I and J, green envelope) that correspond to the membrane 253



14

invaginations shown in Figure 3D. Meanwhile, small opening of the CI was present 254

on the surface of the chloroplast (Fig. 4J, black arrow). In order to visualize the 3D 255

architecture of the CI in more detail, the color of the chloroplast membrane was 256

changed to translucent (Fig. 4J and Supplemental Fig. S5B). The results of this 257

manipulation show that the CIs (yellow) have irregular shapes (Fig. 4J; Supplemental 258

Fig. S5, A and B), with many protrusions present on the CI surface (Fig. 4J; 259

Supplemental Fig. S5B; Supplemental Movies S6-S7), that correspond to the small 260

invaginations around the CIs. These data suggest that the double-membrane bound 261

CIs with openings are also generated by the invagination of the chloroplast 262

membranes. A 3D reconstruction of the chloroplast shown in Figure 4E-H was also 263

performed. In addition to small invaginations on the surface of the chloroplast 264

envelope membranes (Fig. 4, K-M, white arrowheads), the big opening shown in Fig. 265

4E-H (white arrowheads) was, in fact, a deep invagination of chloroplast envelope 266

(Fig. 4K, black arrow; Supplemental Movie S8). Intriguingly, cavern-like 267

invaginations were frequently observed on the surface of the chloroplast (Fig. 4, L 268

and M, white arrows), indicating the irregular appearance of chloroplast membranes 269

under viral attack (Supplemental Movie S8). The experiments described above 270

provide a high-resolution model of chloroplast remodeling occurring during BSMV 271

infection and suggest that the complex invaginations provide sites for virus 272

replication. 273

274

The αa Replication Protein Plays a Major Role in Initiating Chloroplast 275

Remodeling During BSMV Infection 276

To identify BSMV components contributing to chloroplast remodeling, 277

Agrobacterium tumefaciens derivatives harboring pCaBS-α and pCaBS-γ, which are 278

sufficient to support BSMV replication (Jackson et al., 2009), were coinfiltrated into 279

N. benthamiana leaves. TEM analysis was performed at 3 days post inoculation (dpi). 280

As shown in Figure 5, expression of RNAα and RNAγ is sufficient to induce 281

peripheral invaginations and large CIs in chloroplasts (Fig. 5, A and B), and more 282

than 70% of the chloroplasts observed in the infiltrated regions developed structural 283



15

anomalies similar to those of wild-type BSMV infected plants (Fig. 1). Some CIs had 284

large openings to the cytosol (Fig. 5A), in agreement with the feature of the CIs as 285

described in Figure 4. Next, each component encoded by RNAα and RNAγ was 286

transiently expressed in N. benthamiana leaves. In order to achieve high expression 287

levels and easy detection of protein expression, the αa and γa genes were fused to the 288

5′ terminus of the GFP gene and cloned under control of the CBF3 super promoter 289



16

(Chinnusamy et al., 2003; Yang et al., 2010). The results revealed that αa-GFP can 290

induce formation of CIs similar to those observed in BSMV-infected cells (Fig. 5C, 291

white arrows), and the altered chloroplasts accounted for about 20% of the observed 292

chloroplasts. In contrast, CIs were not observed in either γa-GFP or γb-infiltrated 293

leaves (Fig. 5, D and E). Expression of these three proteins was confirmed by Western 294

blotting (data not shown). However, we should point out that despite the ability of 295

αa-GFP to induce CI formation, spherules were difficult to observe in 296

αa-GFP-expressing leaf tissues (Fig. 5C). This may be explained by a requirement for 297

coexpression of the γa, γb or perhaps BSMV RNA components for complete 298

formation of membranous replication vesicles. Irrespective, our results indicate that 299

αa is a major factor mediating chloroplast membrane rearrangements during BSMV 300

infection. 301

302

αa Localizes to the Surface of the Chloroplast 303

Our previous reports revealed that αa-GFP localizes to the chloroplasts (Zhang et al., 304

2017), and our current immuno-EM analyses demonstrate that αa also is targeted to 305

the membranous invaginations (Fig. 2, C-E). To investigate whether αa localizes to 306

the surface or the interior of the chloroplasts, protease protection assays were 307

performed as previously described (Ham et al., 2006). Intact chloroplasts were 308

isolated from N. benthamiana leaves infiltrated with Agrobacterium harboring 309

αa-GFP, AtTOC64-GFP (Breuers et al., 2012) or chloroplast stroma marker 310

ribulose-1,5-bisphosphate carboxylase small subunit GFP fusion (RbcS-GFP) 311

plasmids (Lee et al., 2002), and the chloroplasts were treated with thermolysin in the 312

presence or absence of Triton X-100. The results showed that GFP-fused αa (αa-GFP) 313

was only detected in purified chloroplasts prior to thermolysin incubation (Fig. 6A). 314

Control leaves expressing AtTOC64-GFP, a protein localized to the outer membrane 315

of the chloroplast (Breuers et al., 2012), also had similar results. In contrast, the 316

internal RbcS-GFP protein (Lee et al., 2002) was digested by thermolysin only after 317

the chloroplast membrane was permeabilized by Triton X-100 (Fig. 6A). 318

In addition, a bimolecular fluorescence complementation (BiFC)-based method 319



17

described previously was used to confirm the localization of αa to the cytosolic 320

surface of the chloroplast (Jr et al., 2006; Chen et al., 2016). AtTOC64 is an outer 321

membrane targeting protein whose C-terminal domain is exposed on the cytosolic 322

surface (Qbadou et al., 2007), which provides putative binding to the αa protein. In 323

contrast, contact between the αa and AtTIC40 proteins is unlikely in living cells as 324

AtTIC40 localizes to the chloroplast inner membranes (Chou et al., 2003). These 325



18

protein sequences were engineered into BiFC vectors to provide C-terminal fusions 326

with split YFP derivatives, and transformed into A. tumefaciens. At 3 dpi, confocal 327

laser scanning microscopic analysis of the infiltrated leaf tissues revealed that YFP 328

signals could be observed only for the combinations of AtTOC64 and αa, and the 329

interaction between AtTOC64 and αa occurs on the chloroplast surface, in agreement 330

with the subcellular localization of either AtTOC64 and αa (Fig. 6B). In contrast, 331

coexpression of the αa-nYFP and AtTIC40-cYFP or the αa-cYFP and AtTIC40-nYFP 332

combinations failed to result in fluorescence signals (Fig. 6B), and control leaves 333

coexpressing split YFP-fused AtTOC64 or AtTIC40 with the corresponding empty 334

BiFC vectors, also did not elicit fluorescence signals (Fig. 6B, lower panels). These 335

results indicate that the C-terminus of αa faces the cytoplasm, like AtTOC64, and are 336

consistent with the results of the protease protection assay showing that αa-GFP is 337

sensitive to thermolysin. Furthermore, total protein extracts from N. benthamiana 338

leaves agroinfiltrated with the various BiFC constructs were subjected to Western blot 339

analyses with GFP antibodies to demonstrate that all of the split YFP-fused proteins 340

are expressed in the infiltrated leaf tissues (Supplemental Fig. S6). Collectively, these 341

data demonstrated that αa localizes at the surface of the chloroplasts. 342

343

344



19

DISCUSSION 345

Chloroplasts are one of the most important plant cell organelles, because they are 346

responsible for photosynthesis, synthesis of major phytohormones, participation in 347

defense response, and are crucial for inter-organelle communication. Chloroplast 348

biogenesis is a complex process that is affected by environmental factors such as salt, 349

high temperature, light intensity, and other stress factors (Ballantine and Forde, 1970; 350

Gounaris et al., 1984; Salama et al., 1994). In addition, the subject of 351

chloroplast-virus interplay has been recently attracting more and more attention (Zhao 352

et al., 2016; Bhattacharyya and Chakraborty, 2017). In the present study, electron 353

tomography of the remodeled chloroplasts in BSMV-infected cells provided a model 354

for the 3D architecture of the reorganized chloroplasts, and the viral proteins involved 355

in the BSMV-induced chloroplast structural changes were also investigated. 356

357

BSMV-Induced Chloroplast Rearrangements are Intimately Associated with 358

Virus Replication 359

Lin and Langenberg (1985) first used root tips from BSMV-infected wheat cells to 360

probe the location of dsRNA by IEM, and revealed that peripheral vesicles in 361

proplastids contain dsRNA (Lin and Langenberg, 1985). Our results consistently 362

showed the intimate association of dsRNA with chloroplast peripheral invaginations 363

in BSMV-infected N. benthamiana leaf tissues (Fig. 2, A and B). Our results, in 364

conjunction with those of Lin and Langenberg (1985) suggest that the chloroplast 365

changes induced by BSMV are evolutionarily conserved amongst monocot and dicot 366

families. In addition, BSMV αa replication protein was also found in close proximity 367

to membranous invaginations (Fig. 2, C-E). These data, together with the pore-like 368

openings presented in the 3D architecture of spherules inside these invaginations (Fig. 369

3H), unequivocally verifying the chloroplast membrane-derived spherules are BSMV 370

replication sites. 371

372

3D Reconstructions of the Remodeled Chloroplasts During BSMV Infection 373

Although diverse plant-virus interactions are able to cause chloroplast malformations 374



20

(Zhao et al., 2016), only a limited amount of detailed information is available about 375

structural alterations in chloroplasts during virus infection. Previous studies have 376

shown that Turnip yellow mosaic virus (TYMV) and Wild cucumber mosaic virus 377

(WCMV) infections lead to the ultrastructural changes in chloroplasts, including 378

peripheral vesicles and cytoplasmic invaginations (Ushiyama and Matthews, 1970; 379

Allen, 1972). However, 3D electron tomography revealed that deformation of 380

chloroplasts induced by BSMV is distinct from that of TYMV or WCMV. The 381

BSMV-induced invaginations of the chloroplast inner membrane are larger than those 382

of TYMV and WCMV, and the enlarged space could frequently encompass more than 383

one spherule (Fig. 3), rather than one in the cases of TYMV and WCMV (Ushiyama 384

and Matthews, 1970; Allen, 1972). 385

The 3D architecture of BSMV replication compartments also reveals an intriguing 386

parallel among membranous vesicles induced by distantly related viruses (Kopek et 387

al., 2007; Cao et al., 2015), even though these membranes are derived from different 388

organelles (Verchot, 2011; Romero-Brey and Bartenschlager, 2014). A representative 389

example is the neck-like channel that connect the interior of the spherule to the 390

cytosol. It is assumed that these pore-like openings permit entry of virus and cellular 391

components required for replication, and exit of progeny RNAs to the cytoplasm. The 392

structural similarity among membranous vesicles induced by different viruses 393

supports the hypothesis that an evolutionary conserved mechanism underlies the 394

assembly of virus replication factories. 395

Although the formation of CIs on the chloroplasts has been described in previous 2D 396

EM analyses (McMullen et al., 1978; Lin and Langenberg, 1984, 1985; Torrance et al., 397

2006), the overall architecture of the CIs, and detailed mechanisms whereby CIs are 398

generated during virus infection are obscure. Therefore, electron tomography was 399

performed to reconstruct the 3D structure of BSMV CIs. The results show that 400

abundant virus particles are present in the CIs (Figs. 1 and 2), and that spherules are 401

present at the periphery of the CIs (Supplemental Fig. S4), arguing that replication 402

and packaging of BSMV replicon RNA are tightly coupled processes. Considering the 403

fact that both the BSMV replication proteins αa and γa localize to the chloroplast, 404



21

targeting of viral replication machinery to the chloroplast is initially mediated by the 405

expression of αa and γa, followed by recruitment of the γb protein, BSMV RNAs and 406

diverse host factors to the chloroplast to help membranes to curve, stabilize and 407

activate the replication complexes for replication (Zhang et al., 2017). In addition, a 408

replication-coupled packaging strategy widely utilized in other positive-strand RNA 409

viruses is also applicable to BSMV, as suggested by virus particles present in the 410

chloroplast CIs. 411

FIB-SEM analyses indicated that the BSMV-induced CIs are irregular cavern-like 412

structures with an opening of varied sizes that have invaginated into the chloroplast 413

interior (Fig. 4). Previous studies reported that Potato mop-top virus (PMTV) also 414

elicited formation of cytoplasmic invaginations into chloroplasts during infection 415

(Cowan et al., 2012). Serial sections of the chloroplast in PMTV-infected cells 416

revealed open flask-shaped invaginations (Cowan et al., 2012), similar to those 417

generated by BSMV. However, the PMTV invaginations differ from the 418

BSMV-induced CIs, in that few PMTV particles were observed in these CIs and that 419

peripheral spherules were also absent (Cowan et al., 2012). In addition, in 420

TYMV-infected cells, enlarged membrane spaces between two clumped chloroplasts 421

with large numbers of virus particles inside were observed (Ushiyama and Matthews, 422

1970), which may have similar nature with BSMV-induced CIs. 423

In addition, our studies revealed that the shapes of the BSMV-induced CIs differ and 424

that the sizes of the CIs’ openings varied greatly, from large to small openings (Fig. 4), 425

and in some cases, it was difficult to discern openings of the CIs (Fig. 4 and 426

Supplemental Movie S6). CIs with varied size of openings present in the FIB-SEM 427

analysis allowed us to devise a model whereby invagination of chloroplast 428

membranes proceeds gradually during BSMV infection, leading to the appearance of 429

CIs with diverse morphologies. This can be verified to some extent by the presence of 430

mitochondrion within the CIs (Fig. 4, A-D). 431

Electron tomography analyses of BSMV-induced structural changes in the chloroplast 432

indicated that spherules were often observed at the periphery of the CIs 433

(Supplemental Fig. S4), suggesting a potential relationship during morphogenesis of 434



22

these two structures. In addition, chloroplasts with CIs are more prevalent in the late 435

stage of BSMV infection than in the early infected leaf tissues (data not shown), 436

suggesting that the formation of CIs may be resulted from combined effects of BSMV 437

replication and the physiological responses of the chloroplasts to virus attack. Also, 438

abundant viral particles present inside the CIs might imply that involvement of 439

BSMV virions contributes to some extent to the formation of CIs with diverse 440

morphologies. 441

442

The αa Protein is Essential but Not Sufficient for the Formation of Chloroplast 443

Membrane-Derived Vesicles 444

Virus-induced remodeling of host endomembranes is a complicated process, which 445

has been shown to involve participation of diverse viral and host factors. For example, 446

formation of ER-derived spherules during BMV infection requires the viral 1a’s 447

amphipathic α-helix, helix A, (Liu et al., 2009), and 1a-1a interactions (O'Reilly et al., 448

1997; Diaz et al., 2012). In addition, several host proteins, including 449

membrane-shaping reticulon proteins (Diaz et al., 2010), ESCRT (endosomal sorting 450

complex required for transport) proteins (Diaz et al., 2015), and a lipid 451

synthesis-related Cho2p (choline requiring 2) protein (Zhang et al., 2016), are 452

recruited by 1a to form spherules. 453

Our studies reveal that the αa replication protein has a significant role in rearranging 454

the chloroplast membranes. This finding is in agreement with many previous reports 455

showing that one or more virus-encoded proteins contribute predominately to the 456

ultrastructural changes in cellular endomembrane systems (Schwartz et al., 2002; Liu 457

et al., 2009; Welsch et al., 2009; Romero-Brey et al., 2012). However, this does not 458

mean that the roles of other viral components in remodeling cellular membranes are 459

negligible. In fact, we detected the BSMV αa replication protein and abundant BSMV 460

virions in the CIs and chloroplast-derived spherules (Figs. 1and 2). We also 461

previously detected colocalization of the αa and γa proteins, as well as γb, in 462

chloroplasts (Jackson et al., 2009; Zhang et al., 2017), implying that these viral 463

components, together with the αa, may coordinately contribute to chloroplast 464



23

remodeling and formation of malformed chloroplasts with diverse morphologies (Fig. 465

5). Hence, these findings provide the basis for further studies underway to investigate 466

the detailed molecular mechanisms responsible for the chloroplast remodeling during 467

BSMV infection. 468

In conclusion, our results enhance our understanding of chloroplast biogenesis under 469

stress conditions and present the first 3D reconstruction of aberrant chloroplast 470

structures induced in response to a (+)RNA virus infection, and provide new insights 471

into the assembly of (+)RNA virus replication complex. 472

473

MATERIALS AND METHODS 474

475

Plasmids Construction 476

All plasmids were constructed according to the standard molecular cloning methods 477

(Sambrook and Russell, 2001). For transient expression assays, the γa and γb genes 478

were amplified from pCaBS-γ (Yuan et al., 2011; Hu et al., 2015) and cloned into 479

pSuper1300-GFP containing the CBF3 super promoter (Chinnusamy et al., 2003; 480

Yang et al., 2010) and pGD as described previously (Zhang et al., 2017). For BiFC 481

assays, AtTOC64 and AtTIC40 were cloned from the plasmids AtTOC64-GFP and 482

AtTIC40-GFP (Breuers et al., 2012), respectively, and inserted into pSPYCE-35S or 483

pSPYNE-35S (Walter et al., 2004). The plasmids pSPYCE-35S-NbrbcL and 484

pSPYNE-35S-NbrbcL were described in a previous report (Cao et al., 2015). For 485

protease protection assays, the NbRbcS gene was amplified from N. benthamiana 486

cDNA and inserted into pSuper1300-GFP to generate pSuper1300-NbRbcS-GFP. 487

Primers used for constructing these plasmids are listed in Supplemental Table S1, and 488

sequence analyses were performed to confirm the accuracy of all plasmids. 489

490

Transmission Electron Microscopy (TEM) 491

Transmission electron microscopy was performed as described previously (Cao et al., 492

2015). Briefly, N. benthamiana leaves were cut into pieces and fixed overnight at 4°C 493

in fixation buffer (2.5% glutaraldehyde, 0.05 M phosphate, pH 7.2). Samples were 494



24

then washed for three times with fixation buffer followed by post-fixation in 2% 495

osmium tetroxide at 4°C for 2 h. After dehydration in a graded ethanol series (50%, 496

70%, 80%, 90%, 95% and 100%), the tissue samples were embedded in Spurr’s resin. 497

Ultrathin sections (70-90 nm) were cut using a Leica EM UC7 ultramicrotome, and 498

sequentially stained with uranyl acetate for 20 min and Reynolds’ lead citrate for 5 499

min. The sections were then viewed with a Hiltachi H-7650 or a JEM-1230 500

transmission electron microscope operated at 80 kV. 501

502

Immunoelectron Microscopy 503

Immunogold labeling was performed according to previously described method with 504

minor modifications (Liu et al., 2015). Leaf tissues from healthy or BSMV-infected N. 505

benthamiana were vacuum-infiltrated with a mixture of 3% formaldehyde, 0.1% 506

glutaraldehyde, 4% sucrose in 0.1 M phosphate buffer (pH 7.2), and fixed at 4°C for 507

2-3 h. After washing with phosphate buffer, the samples were dehydrated in 508

increasing ethanol concentrations (30%, 50%, 70%, 80%, 95%, and 100%), infiltrated 509

in increasing concentrations of Lowicryl K4M resin (50 %, 75 % in methanol, and 510

pure resin), and polymerized under UV light (360 nm) for 72 h at -20°C, and then for 511

48 h at room temperature. After polymerization, ultrathin sections were cut from 512

blocks and collected on Formvar-coated nickel grids. The grids were incubated in 513

blocking solution [0.01 M PBS (pH 7.2) with 1% BSA, 0.05% Triton X-100, 0.05% 514

Tween-20] for 5 min at room temperature to reduce nonspecific binding, and 515

incubated with primary mouse monoclonal anti-dsRNA antibody (J2, English & 516

Scientific Consulting Kft), rabbit polyclonal anti-CP or anti-αa antibodies, 517

respectively. Polyclonal αa-specific antibodies were prepared from the sera of rabbits 518

immunized with the purified αa protein helicase domain (Zhang et al., 2017). After 519

washing six times with 0.01 M PBS buffer, the grids were incubated with goat 520

anti-mouse or goat anti-rabbit secondary antibodies conjugated with 10 nm gold 521

particles, followed by rinsing with 0.01 M PBS buffer. Finally, sections were stained 522

with uranyl acetate and Reynolds’ lead citrate prior to viewing with a Hiltachi H-7650 523

or JEM-1230 transmission electron microscope. 524



25

525

Transmission Electron Tomography 526

All procedures were performed as described previously with minor modification 527

(Kang et al., 2011; Toyooka and Kang, 2014). Serial sections (250 nm) were cut from 528

blocks of BSMV-infected or control N. benthamiana leaf tissues, and collected on 529

slot-grids followed by staining with uranyl acetate and lead citrate as described above. 530

Fiducial markers consisting of 15 nm gold particles were deposited on both sides of 531

the sections to facilitate image tracing and alignment. For BSMV-infected and control 532

samples, double-axis tilt series was collected with a cooled slow-scan 533

charge-coupled–device (CCD) camera (4K Eagle) of FEI TF20 (200 kV) at 1.5° tilt 534

increments from -60° to 60° to obtain 81 images. After one double-axis tilt series 535

finished, the grid was turned 90° and started the second double-axis tilt series. For 536

each tilt series, two sections were collected and joined using the IMOD software 537

package (Kremer et al., 1996), with 324 images were recorded for two sections in one 538

sample in total. The magnification was 14,500×, corresponding to a pixel size of 1.50 539

nm. The 3D surface renderings of the tomograms were performed with the IMOD 540

software package (http://bio3d.colorado.edu/imod/doc/3dmodguide.html) 541

542

FIB-SEM Tomography 543

Samples for FIB-SEM analysis were prepared as described for TEM with minor 544

modifications. To enhance the contrast, samples were post-fixed in a mixture of 2% 545

osmium tetroxide and 1.5% potassium hexacyanoferrate at 4°C for 2 h, followed by 546

block staining with 2% aqueous uranyl acetate overnight at 4°C. Dehydration and 547

embedding were performed as described above. 548

For FIB-SEM observations, blocks were trimmed to obtain a smooth flat surface, and 549

interested areas were exposed, and the samples were glued on a stage and sputtered 550

with gold (HITACHI, E1010) for 90 s, followed by placing in the FIB-SEM 551

microscope (FEI Helios NanoLab G3 UC). A 500 nm thick layer of platinum was 552

deposited on the top surface of the block with the gas injector system (GIS). The 553

focused gallium ion beam was used with the slice thickness of 50 nm, and an 554



26

accelerating voltage of 30 kV (a current of 9.3 nA). After FIB milling, the freshly 555

milled block face was tilted to 7° in order to be vertical to the electron beam. The 556

accelerating voltage of electron beam was 2 kV and the current to 0.4 nA (10 μs pixel 557

dwell time). Images were taken at a magnification of 11,477× with a resolution of 558

4096 × 3536 pixels, and the horizontal field of view was 24.1 μm corresponding to a 559

pixel size of 5.88 nm. The SEM images were aligned, processed and 3D 560

surface-rendered using the IMOD software package 561

(http://bio3d.colorado.edu/imod/doc/3dmodguide.html). 562

563

Agroinfiltration 564

Infiltration of A. tumefaciens into the N. benthamiana was described previously (Yang 565

et al., 2000). To enhance protein expression, suspensions of Agrobacterium carrying 566

plasmids were often co-infiltrated with Agrobacterium harboring the p19 expression 567

cassette. At 3 dpi, the infiltrated leaves were viewed under confocal microscopy or 568

used for transmission electron microscopic analysis. 569

570

Confocal Laser Scanning Microscopy 571

Confocal analysis was performed as described previously (Cao et al., 2015). YFP or 572

chlorophyll autofluorescence was observed using an Olympus FV1000 laser scanning 573

confocal microscope with an excitation wavelength of 514 or 633 nm, respectively. 574

Images were processed with Imaris 7.4.2 software (Bitplane). 575

576

Protease Protection Assays 577

Protease protection assays were performed according to previously described methods 578

with minor modifications (Ham et al., 2006). Briefly, intact chloroplasts were isolated 579

from N. benthamiana leaves as described previously (Ling and Jarvis, 2015). 580

Chloroplast yields were calculated using a unit chlorophyll basis. 10 μl of chloroplast 581

suspension was added to 1 ml of 80% acetone prior to centrifugation at 3,000 g for 2 582

min. Absorbance of the supernatant was measured at 652 nm with a 583

spectrophotometer (METASH) and inserted into the Sigma chloroplast isolation kit 584



27

formula: mg chlorophyll/ml = A652×100/36. To obtain the same concentration of 585

chloroplast suspension, chloroplast suspension was diluted to 1 mg/ml chlorophyll 586

with the treating buffer containing 1 mM CaCl2, 300 mM sorbitol, 50 mM 587

HEPES-KOH (pH 8.0). 200 μg thermolysin was added for every 1 mg chlorophyll in 588

treating buffer with or without the addition of 0.5% Triton X-100 followed by 589

incubation at 25°C for 1 h. After thermolysin treatment, protease inhibitor cocktail 590

(Sigma) and 5 mM EDTA were added to terminate the reaction. For the treatment 591

with Triton X-100, the suspension was directly subjected to Western blot analysis. For 592

the treatment without Triton X-100, intact chloroplasts were reisolated using 40%/80% 593

Percoll density gradient centrifugation followed by Western blot analyses. 594

595

ACKNOWLEDGMENTS 596

597

We would like to thank Drs. Jialin Yu, Chenggui Han, Xianbing Wang, and Ying 598

Wang at China Agricultural University for valuable discussions during the course of 599

this work. We also thank Dr. Andrew O. Jackson (University of California-Berkeley, 600

USA) for his great help in editing and proofreading of the manuscript, and Dr. Jian 601

Hong (Zhejiang University, China) for helpful suggestions on our project. We thank 602

Drs. Ying Li and Xiaomin Li at Tsinghua University for technical assistance of 603

preparing the ultrathin sections and FIB-SEM analysis, and Drs. Wei Ding, Jianguo 604

Zhang and Lei Sun (HPC-Service Station in Center for Biological Imaging, Institute 605

of Biophysics, Chinese Academy of Sciences) for their help in FIB-SEM analysis and 606

data processing. We thank Dr. Andreas P.M. Weber (Heinrich Heine University 607

Düsseldorf, Germany) for providing the AtTOC64-GFP and AtTIC40-GFP plasmids. 608

The authors thank the editor and three anonymous reviewers for their constructive 609

comments and suggestions on earlier drafts of this article. 610

611

FIGURE LEGENDS 612

Figure 1. Ultrastructural changes in chloroplasts during BSMV infection of N. 613

benthamiana. 614



28

A, Healthy N. benthamiana leaves served as a control. B-D, Deformed chloroplasts in 615

BSMV-infected N. benthamiana leaf tissues. B, Cytoplasmic invaginations (CIs) 616

present in chloroplasts within a BSMV-infected cell. C, Virus-like particles (VLPs, 617

black arrows) were present within a CI, and membrane invaginations were observed 618

at both the periphery of CI and the chloroplast envelope membranes (white arrows 619

and arrowheads). D, Invaginations present around the chloroplast envelope (white 620

arrowheads). Inset area shows magnification of the spherule that was occasionally 621

observed inside the invagination. Chl, chloroplast; S, starch granule; CI, cytoplasmic 622

invagination; VLP, virus-like particle; CW, cell wall. Scale bars, 500 nm. 623

624

Figure 2. Immunoelectron microscopy of viral dsRNA and proteins in 625

BSMV-infected N. benthamiana cells. 626

A-B, Immunogold labeling of dsRNA in BSMV-infected N. benthamiana cells. Insets 627

I and II show magnifications of the corresponding boxed regions. C-E, αa localization 628

at envelope membranes (white arrowheads), small invaginations (boxed regions), and 629

CI periphery (white arrowheads) in BSMV-infected N. benthamiana cells. Black 630

arrows point to virus-like particles. Boxed areas show the invaginations at the CI 631

periphery. F-G, CP-specific antiserum showed specific labeling of virus-like particles 632

(black arrows) in the cytoplasm and CIs. Note: OsO4 fixation of the leaf tissues was 633

omitted to preserve antigenicity of target molecules. Hence, the fine structure of 634

cellular membranes could not be unambiguously visualized. Chl, chloroplast; CI, 635

cytoplasmic invagination; VLP, virus-like particle; CW, cell wall. Scale bars, 200 nm. 636

637

Figure 3. Three-dimensional visualization of remodeled chloroplast membranes 638

in BSMV-infected cells by transmission electron tomography. 639

A, Representative tomogram slice generated from a 250-nm-thick section of 640

systemically infected N. benthamiana leaves. BSMV-induced peripheral invaginations 641

and large CI can be observed in chloroplast. Boxed area shows the invaginations at 642

the chloroplast periphery. B and C, Different slices of the boxed area shown in A. 643

Yellow arrowheads show peripheral invaginations with internal spherules. D, 3D 644



29

model of chloroplast membranes shown in A. Light blue, outer chloroplast membrane; 645

translucent white, inner chloroplast membrane; light yellow, spherules derived from 646

the outer membrane; white arrowheads, peripheral invaginations of the chloroplast. E, 647

Close-up view of the area indicated by white arrowheads in D without showing the 648

outer chloroplast membrane. F, Close-up view of the area indicated by white 649

arrowheads in D without showing the inner chloroplast membrane. G, Close-up view 650

of the area indicated by white arrowheads in D showing both the outer and inner 651

chloroplast membranes. H, A 90° rotation of G highlighting spherules connections 652

(arrowhead and black dashed circle) to the cytoplasm. CI, cytoplasmic invagination; 653

Scale bars, 200 nm. This tomogram is shown in Supplemental Movies S2-S4. 654

655

Figure 4. Three-dimensional visualization of BSMV-induced cytoplasmic 656

invaginations by FIB-SEM-based electron tomography. 657

A-D, Four different slices from the same chloroplast selected to illustrate CI 658

structures. Arrowheads indicate 3D variations in the CI opening. E-H, A series of 659

slices from another chloroplast showing morphological changes of the CI. 660

Arrowheads indicate 3D variations in the CI opening. I-J, A 3D surface rendering of 661

the chloroplast tomogram in A-D. Green, chloroplast; Yellow, CI. To emphasize the 662

CI (yellow) inside the chloroplast, the appearance of chloroplast shown in I was 663

changed to translucent (J). White arrowheads indicate chloroplast envelope 664

invaginations similar to those in Fig. 3D; black arrow point to the CI opening. The 665

image inset J is an enlarged view of the CI. Note: the 3D model in I-J represent partial 666

3D architecture of the chloroplast shown in A-D, see Supplemental Movies S6-S7 for 667

the complete 3D model. K-M, Different views of the 3D model corresponding to the 668

chloroplast shown in panels E-H. White arrowheads indicate chloroplast envelope 669

invaginations similar to those in Fig. 3D; black arrow point to the CI apertures; white 670

arrows indicate cavern-like invaginations present on the surface of the chloroplasts. 671

This tomogram is shown in Supplemental Movie S8. Chl, chloroplast; CI, 672

cytoplasmic invagination; Mt, mitochondria. Scale bars, 500 nm. 673

674



30

Figure 5. Function of αa in chloroplast remodeling during BSMV infection. 675

Transmission electron microscopy (TEM) of agroinfiltrated leaf tissues infected with 676

BSMV. A-B, TEM of N. benthamiana leaf tissues coexpressing BSMV RNAα and 677

RNAγ stands. Note the altered chloroplast membrane structures like cytoplasmic 678

invaginations and peripheral invaginations. Inset: enlarged box in A shows 679

cytoplasmic invaginations with openings facing the cytoplasm. C-E, TEM of N. 680

benthamiana leaf tissues agroinfiltrated with bacteria harboring αa-GFP (C), γa (D), 681

and γb (E) plasmids. Arrows indicate the CIs. Chl, chloroplast; CI, cytoplasmic 682

invagination; CW, cell wall; Mt, mitochondria; Nu, nucleus; Ag, Agrobacteria in 683

intercellular spaces. Scale bars, 500 nm. 684

685

Figure 6. αa localizes to the surface of the chloroplasts. 686

A, Protease protection assay to determine chloroplast localization of αa. Intact 687

chloroplasts were isolated from N. benthamiana leaves expressing αa-GFP, 688

AtTOC64-GFP or RbcS-GFP, and subjected to thermolysin digestion with or without 689

Triton X-100 treatment. Protein samples were prepared from 5 μg chlorophyll 690

equivalent of chloroplasts, and subjected to Western blot analyses using antibodies 691

specified on the right of the panels. Phosphoenolpyruvate carboxylase (PEPC), a 692

cytoplasmic enzyme, served as a control to assess cytosolic contaminations of isolated 693

chloroplasts. Arrowheads indicate the specific band of the target protein. B, BiFC 694

analysis of interactions between the BSMV αa protein and the chloroplast outer 695

membrane protein AtTOC64 or the inner membrane protein AtTIC40. YFP signals are 696

depicted as a false-green color and chlorophyll autofluorescence is displayed in red. 697

Scale bars, 10 μm. 698

699

Supplemental Data 700

Supplemental Table S1. List of primers used for plasmid constructions. 701

Supplemental Table S2. List of primers used for RT-PCR. 702

Supplemental Figure S1. Ultrastructural changes in BSMV-infected N. 703

benthamiana cells. 704



31

Supplemental Figure S2. Immunoelectron microscopic analysis of healthy N. 705

benthamiana leaf tissues. 706

Supplemental Figure S3. Analysis of viral components in agroinfiltrated N. 707

benthamiana leaves and isolated chloroplasts. 708

Supplemental Figure S4. Transmission electron tomography showing 709

three-dimensional visualization of the partial structure of BSMV-induced 710

cytoplasmic invaginations. 711

Supplemental Figure S5. 3D model of the BSMV-induced cytoplasmic 712

invaginations generated from FIB-SEM-based electron tomography. 713

Supplemental Figure S6. Western blot analysis of the total protein samples from 714

N. benthamiana leaves expressing split YFP-fused proteins. 715

Supplemental Movies S1-S2. Representative electron tomograms of chloroplast 716

in healthy (S1) and BSMV-infected (S2) N. benthamiana cells. 717

Supplemental Movies S3-S5. 3D surface rendering of rearranged chloroplast 718

envelope membranes and the CI based on the transmission electron tomograms. 719

Supplemental Movies S6-S8. 3D surface rendering of BSMV-induced 720

cytoplasmic invaginations based on the merged FIB-SEM images. 721

722

723

Supplemental Table S1. List of primers used for plasmid constructions. 724

725

Supplemental Table S2. List of primers used for RT-PCR. 726

727

Supplemental Figure S1. Ultrastructural changes in BSMV-infected N. 728

benthamiana cells. 729

A, Membranous inclusion induced by BSMV in N. benthamiana cells. B, 730

Mitochondria were elongated during BSMV infection. C, Cytoplasm containing a 731

large number of virus-like particles protrudes into the vacuole. Chl, chloroplast; IN, 732

membranous inclusion; Nu, nucleus; Cyt, cytoplasm; Vac, vacuole; VLP, virus-like 733

particle; CW, cell wall; Mt, mitochondria. Scale bars, 1 μm. 734



32

735

Supplemental Figure S2. Immunoelectron microscopic analysis of healthy N. 736

benthamiana leaf tissues. 737

Healthy N. benthamiana leaves were subjected to immunogold labeling with 738

antibodies against dsRNA (A), αa (B), or CP (C). Note: To preserve the antigenicity 739

of the target molecules, OsO4 fixation of the leaf tissues was omitted. Thus, the fine 740

structure of cellular membrane structures could not be visualized unambiguously. Chl, 741

chloroplast; CW, cell wall. Scale bars, 200 nm. 742

743

Supplemental Figure S3. Analysis of viral components in agroinfiltrated N. 744

benthamiana leaves and isolated chloroplasts. 745

A, Western blot analysis of total protein extracts (Total) from mock- (M, lane 1) and 746

BSMV-inoculated (V, lane 3) leaves or that from isolated chloroplasts (Chl, lanes 2 747

and 4). Antibodies used for Western blot are indicated on the right of each panel. 748

Sizes (in kDa) of molecular weight markers (Mr) are shown on the left. B, RT-PCR 749

analysis of RNAs extracted from the leaves (top panels) or isolated chloroplasts 750

(bottom panels). Agroinfiltrated N. benthamiana leaf samples were further used for 751

chloroplast isolations. Total RNAs were then extracted from the leaves or isolated 752

chloroplasts, and subjected to RT-PCR analysis using the primers listed in 753

Supplemental Table S2. The psbC and 18S rRNA genes were served as the chloroplast 754

and cytoplasmic markers, respectively. BSMV(+) and BSMV(-) denote viral plus- and 755

minus-strand RNA. Sizes (in bp) of the DNA markers are indicated on the left. 756

757

Supplemental Figure S4. Transmission electron tomography showing 758

three-dimensional visualization of the partial structure of BSMV-induced 759

cytoplasmic invaginations. 760

A-B, Representative tomogram slices generated from a 250-nm-thick section of 761

systemically infected N. benthamiana leaves. Yellow arrowheads indicated membrane 762

invaginations at the periphery of the CI. C-D, 3D models of the CI shown in A-B. 763

Light blue, inner CI membrane; translucent white, outer CI membrane; light yellow, 764



33

spherules derived from the inner CI membrane. E, A close-up view of the spherules at 765

the periphery of the CI that have eliminated the chloroplast inner membrane. F, A 90° 766

rotation of E to highlight the pore-like openings (yellow arrowheads) of the spherules. 767

The inset in F shows enlarged image of the pore-like openings. Scale bars, 200 nm. 768

This tomographic reconstruction is shown in Supplemental Movie S5. 769

770

Supplemental Figure S5. 3D model of the BSMV-induced cytoplasmic 771

invaginations generated from FIB-SEM-based electron tomography. 772

To highlight the CI (yellow) inside the chloroplast, the appearance of chloroplast 773

shown in A was changed to translucent in panel B. White arrowheads point to the 774

chloroplast envelope invaginations described in Fig. 3D. Note: the 3D models 775

presented in panels A and B show partial 3D architecture of the remodeled chloroplast 776

shown in Fig. 4A-D, see Supplemental Movies S6-S7 for the complete 3D model. 777

Scale bars, 500 nm. 778

779

Supplemental Figure S6. Western blot analysis of the total protein samples from 780

N. benthamiana leaves expressing split YFP-fused proteins. 781

N. benthamiana leaves were agroinfiltrated with various BiFC constructs as indicated 782

above the gel lanes, and leaf samples were collected for Western blot analysis at 3 dpi. 783

Sizes (in kDa) of molecular weight markers (Mr) are shown on the left and antibodies 784

used for detection are shown on the right. Arrowheads indicate the specific bands of 785

the target proteins. 786

787

Supplemental Movies S1-S2. Representative electron tomograms of chloroplast 788

in healthy (S1) and BSMV-infected (S2) N. benthamiana cells. 789

790

Supplemental Movies S3-S5. 3D surface rendering of rearranged chloroplast 791

envelope membranes and the CI based on the transmission electron tomograms. 792

The outer membrane of chloroplast is colored light blue and inner membrane of 793

chloroplast translucent white. Spherules derived from the outer membrane are colored 794



34

light yellow. These movies correspond to Figure 3 and Supplemental Figure S4. 795

796

Supplemental Movies S6-S8. 3D surface rendering of BSMV-induced 797

cytoplasmic invaginations based on the merged FIB-SEM images. Chloroplast is 798

colored green and CI is colored yellow. These movies correspond to Figure 4 and 799

Supplemental Figure S5. 800

801

802



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Boon JAD, Diaz A, Ahlquist P (2010) Cytoplasmic viral replication complexes. Cell Host Microbe 8: 77-85.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Breuers FKH, Bräutigam A, Geimer S, Welzel UY, Stefano G, Renna L, Brandizzi F, Weber APM (2012) Dynamic remodeling of theplastid envelope membranes-a tool for chloroplast envelope in vivo localizations. Front Plant Sci 3: 7-7


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Carroll TW (1970) Relation of Barley stripe mosaic virus to plastids. Virology 42: 1015-1022Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Chen YL, Chen LJ, Li HM (2016) Polypeptide transport-associated domains of the Toc75 channel protein are located in theintermembrane space of chloroplasts. Plant Physiol 172: 235-243


Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong X, Agarwal M, Zhu JK (2003) ICE1: a regulator of cold-induced transcriptome andfreezing tolerance in Arabidopsis. Genes Dev 17: 1043-1054


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Cowan GH, Roberts AG, Chapman SN, Ziegler A, Savenkov EI, Torrance L (2012) The Potato mop-top virus TGB2 protein and viral RNAassociate with chloroplasts and viral infection induces inclusions in the plastids. Front Plant Sci 3: 290


Daum B, Nicastro D, Austin J, 2nd, McIntosh JR, Kuhlbrandt W (2010) Arrangement of photosystem II and ATP synthase in chloroplastmembranes of spinach and pea. Plant Cell 22: 1299-1312


De Castro IF, Fernández JJ, Barajas D, Nagy PD, Risco C (2017) Three-dimensional imaging of the intracellular assembly of a functionalviral RNA replicase complex. J Cell Sci 130: 260-268


Diaz A, Gallei A, Ahlquist P (2012) Bromovirus RNA replication compartment formation requires concerted action of 1a's self-interactingRNA capping and helicase domains. J Virol 86: 821-834


Diaz A, Wang X, Ahlquist P (2010) Membrane-shaping host reticulon proteins play crucial roles in viral RNA replication compartmentformation and function. Proc Natl Acad Sci USA 107: 16291-16296


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http://www.ncbi.nlm.nih.gov/pubmed?term=Chou ML%2C Fitzpatrick LM%2C Tu SL%2C Budziszewski G%2C Potter%2DLewis S%2C Akita M%2C Levin JZ%2C Keegstra K%2C Li HM %282003%29 Tic40%2C a membrane%2Danchored co%2Dchaperone homolog in the chloroplast protein translocon%2E EMBO J 22%3A 2970%2D2980&dopt=abstract

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http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Chou&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Cowan GH%2C Roberts AG%2C Chapman SN%2C Ziegler A%2C Savenkov EI%2C Torrance L %282012%29 The Potato mop%2Dtop virus TGB2 protein and viral RNA associate with chloroplasts and viral infection induces inclusions in the plastids%2E Front Plant Sci 3%3A 290&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Cowan GH, Roberts AG, Chapman SN, Ziegler A, Savenkov EI, Torrance L (2012) The Potato mop-top virus TGB2 protein and viral RNA associate with chloroplasts and viral infection induces inclusions in the plastids. Front Plant Sci 3: 290

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Cowan&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The Potato mop-top virus TGB2 protein and viral RNA associate with chloroplasts and viral infection induces inclusions in the plastids.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The Potato mop-top virus TGB2 protein and viral RNA associate with chloroplasts and viral infection induces inclusions in the plastids.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Cowan&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Daum B%2C Nicastro D%2C Austin J%2C 2nd%2C McIntosh JR%2C Kuhlbrandt W %282010%29 Arrangement of photosystem II and ATP synthase in chloroplast membranes of spinach and pea%2E Plant Cell 22%3A 1299%2D1312&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Daum B, Nicastro D, Austin J, 2nd, McIntosh JR, Kuhlbrandt W (2010) Arrangement of photosystem II and ATP synthase in chloroplast membranes of spinach and pea. Plant Cell 22: 1299-1312

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Daum&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Arrangement of photosystem II and ATP synthase in chloroplast membranes of spinach and pea&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Arrangement of photosystem II and ATP synthase in chloroplast membranes of spinach and pea&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Daum&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=De Castro IF%2C Fern�ndez JJ%2C Barajas D%2C Nagy PD%2C Risco C %282017%29 Three%2Ddimensional imaging of the intracellular assembly of a functional viral RNA replicase complex%2E J Cell Sci 130%3A 260%2D268&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=De Castro IF, Fern�ndez JJ, Barajas D, Nagy PD, Risco C (2017) Three-dimensional imaging of the intracellular assembly of a functional viral RNA replicase complex. J Cell Sci 130: 260-268

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=De&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Three-dimensional imaging of the intracellular assembly of a functional viral RNA replicase complex&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Three-dimensional imaging of the intracellular assembly of a functional viral RNA replicase complex&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=De&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Diaz A%2C Gallei A%2C Ahlquist P %282012%29 Bromovirus RNA replication compartment formation requires concerted action of 1a%27s self%2Dinteracting RNA capping and helicase domains%2E J Virol 86%3A 821%2D834&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Diaz A, Gallei A, Ahlquist P (2012) Bromovirus RNA replication compartment formation requires concerted action of 1a's self-interacting RNA capping and helicase domains. J Virol 86: 821-834

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Diaz&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Bromovirus RNA replication compartment formation requires concerted action of 1a's self-interacting RNA capping and helicase domains&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=Diaz A%2C Wang X%2C Ahlquist P %282010%29 Membrane%2Dshaping host reticulon proteins play crucial roles in viral RNA replication compartment formation and function%2E Proc Natl Acad Sci USA 107%3A 16291%2D16296&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Harak C%2C Lohmann V %282015%29 Ultrastructure of the replication sites of positive%2Dstrand RNA viruses%2E Virology 479%2D480%3A 418%2D433&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Yang H%2C Shi Y%2C Liu J%2C Guo L%2C Zhang X%2C Yang S %282010%29 A mutant CHS3 protein with TIR%2DNB%2DLRR%2DLIM domains modulates growth%2C cell death and freezing tolerance in a temperature%2Ddependent manner in Arabidopsis%2E Plant J 63%3A 283%2D296&dopt=abstract

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http://scholar.google.com/scholar?as_q=A mutant CHS3 protein with TIR-NB-LRR-LIM domains modulates growth, cell death and freezing tolerance in a temperature-dependent manner in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yang&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

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three-dimensional analysis of chloroplast …...35 y.z.), the research grants council of hong kong...

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