Comparative Genomics of the Small Heat Shock Protein Family in Angiosperms

doi:10.11983/CBB20209

Abstract

Abstract: Small heat shock protein (sHSP) can respond to environmental stresses and regulate plant growth and development. In this study, 33 NcsHSPs, 24 OssHSPs, 17 AtsHSPs and 47 VvsHSPs were found in waterlily, rice, Arabidopsis, and grape, respectively. The sHSP family can be divided into 12 subfamilies, and different subfamily had different number of sHSP members, conserved motifs, gene structures and number of duplicated genes. Then, 12 gene duplication events in tle sHSP fanily were identified from 4 model angiosperms of sHSP family. The segmental and tandem duplication events were related to the gene expansion in the sHSP family, and the segmental duplication events occurred earlier than the tandem duplication events. Moreover, sHSP members in Arabidopsis and grape had the highest orthologous similarity, followed by sHSP members in waterlily and grape. Furthermore, sHSP family in angiosperms evolved towards sHSP members with smaller length of amino acid, lower molecular weight, simpler gene structure, and concentrated chromosomal localization. Besides, some sHSP members may be related to plant growth and development in waterlily, rice, Arabidopsis, and grape. Above all, these results could lay vital foundations on comparative genomics of the sHSP family in four model angiosperms and advance the sHSP family in other angiosperms.

Key words: sHSP family, comparative genomics, expansion, gene expression

Kai Fan, Fangting Ye, Zhijun Mao, Xinfeng Pan, Zhaowei Li, Wenxiong Lin. Comparative Genomics of the Small Heat Shock Protein Family in Angiosperms[J]. Chinese Bulletin of Botany, 2021, 56(3): 245-261.

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URL: https://www.chinbullbotany.com/EN/10.11983/CBB20209

https://www.chinbullbotany.com/EN/Y2021/V56/I3/245

Figures/Tables 10

References 47

1	何福林, 张斌 (2019). 银杏(Ginkgo biloba) GbHsp20基因家族的鉴定及系统进化分析. 分子植物育种 17, 7368-7376.
2	黄祥富, 黄上志, 傅家瑞 (1999). 植物热激蛋白的功能及其基因表达的调控. 植物学通报 16, 530-536.
3	栗振义, 龙瑞才, 张铁军, 杨青川, 康俊梅 (2016). 植物热激蛋白研究进展. 生物技术通报 32(2), 7-13.
4	刘德立 (1996). 植物热激蛋白及其功能. 植物学通报 13, 14-19.
5	张宁, 姜晶, 史洁玮 (2017). 番茄HSP20基因家族的全基因组鉴定、系统进化及表达分析. 沈阳农业大学学报 48, 137-144.
6	张奇艳, 雷忠萍, 宋银, 海江波, 贺道华 (2019). 陆地棉扩展蛋白基因的鉴定与特征分析. 中国农业科学 52, 3713-3732.
7	Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004). The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4, 10. DOI URL
8	Chen CJ, Chen H, Zhang Y, Thomas HR, Frank MH, He YH, Xia R (2020). TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13, 1194-1202. DOI URL
9	Dafny-Yelin M, Tzfira T, Vainstein A, Adam Z (2008). Non-redundant functions of sHSP-CIs in acquired thermotolerance and their role in early seed development in Arabidopsis. Plant Mol Biol 67, 363-373. DOI PMID
10	Fan K, Chen YR, Mao ZJ, Fang Y, Li ZW, Lin WW, Zhang YQ, Liu JP, Huang JW, Lin WX (2020a). Pervasive duplication, biased molecular evolution and comprehensive functional analysis of the PP2C family in Glycine max. BMC Genomics 21, 465. DOI URL
11	Fan K, Mao ZJ, Zheng JX, Chen YR, Li ZW, Lin WW, Zhang YQ, Huang JW, Lin WX (2020b). Molecular evolution and expansion of the KUP family in the allopolyploid cotton species Gossypium hirsutum and Gossypium barbadense. Front Plant Sci 11, 545042. DOI URL
12	Fan K, Shen H, Bibi N, Li F, Yuan SN, Wang M, Wang XD (2015). Molecular evolution and species-specific expansion of the NAP members in plants. J Integr Plant Biol 57, 673-687. DOI URL
13	Fan K, Wang M, Miao Y, Ni M, Bibi N, Yuan SN, Li F, Wang XD (2014). Molecular evolution and expansion analysis of the NAC transcription factor in Zea mays. PLoS One 9, e111837. DOI URL
14	Guo CL, Guo RR, Xu XZ, Gao M, Li XQ, Song JY, Zheng Y, Wang XP (2014). Evolution and expression analysis of the grape (Vitis vinifera L.) WRKY gene family. J Exp Bot 6, 1513-1528.
15	Guo LM, Li J, He J, Liu H, Zhang HM (2020). A class I cytosolic HSP20 of rice enhances heat and salt tolerance in different organisms. Sci Rep 10, 1383. DOI URL
16	Guo M, Liu JH, Lu JP, Zhai YF, Wang H, Gong ZH, Wang SB, Lu MH (2015). Genome-wide analysis of the CaHsp20 gene family in pepper: comprehensive sequence and expression profile analysis under heat stress. Front Plant Sci 6, 806.
17	Ji XR, Yu YH, Ni PY, Zhang GH, Guo DL (2019). Genome-wide identification of small heat-shock protein (HSP20) gene family in grape and expression profile during berry development. BMC Plant Biol 19, 433. DOI URL
18	Jiao YN, Leebens-Mack J, Ayyampalayam S, Bowers JE, McKain M, McNeal J, Rolf M, Ruzicka DR, Wafula E, Wickett NJ, Wu XL, Zhang Y, Wang J, Zhang YT, Carpenter EJ, Deyholos MK, Kutchan TM, Chanderbali AS, Soltis PS, Stevenson DW, McCombie R, Pires JC, Wong GKS, Soltis DE, DePamphilis DW (2012). A genome triplication associated with early diversification of the core eudicots. Genome Biol 13, R3. DOI URL
19	Key JL, Lin CY, Chen YM (1981). Heat shock proteins of higher plants. Proc Natl Acad Sci USA 78, 3526-3530. DOI URL
20	Lamesch P, Berardini TZ, Li DH, Swarbreck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander DL, Garcia-Hernandez M, Karthikeyan AS, Lee CH, Nelson WD, Ploetz L, Singh S, Wensel A, Huala E (2012). The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res 40, D1202-D1210. DOI URL
21	Li JB, Zhang J, Jia HX, Li Y, Xu XD, Wang LJ, Lu MZ (2016). The Populus trichocarpa PtHSP17.8 involved in heat and salt stress tolerances. Plant Cell Rep 35, 1587-1599. DOI URL
22	Li JB, Zhang J, Jia HX, Yue ZQ, Lu MZ, Xin XB, Hu JJ (2018). Genome-wide characterization of the sHsp gene family in Salix suchowensis reveals its functions under different abiotic stresses. Int J Mol Sci 19, 3246. DOI URL
23	Li Q, Zhang N, Zhang LS, Ma H (2015). Differential evolution of members of the rhomboid gene family with conservative and divergent patterns. New Phytol 206, 368-380. DOI URL
24	Ma W, Guan XY, Li J, Pan RH, Wang LY, Liu FJ, Ma HY, Zhu SJ, Hu J, Ruan YL, Chen XY, Zhang TZ (2019). Mitochondrial small heat shock protein mediates seed germination via thermal sensing. Proc Natl Acad Sci USA 116, 4716-4721. DOI URL
25	Ma W, Zhao T, Li J, Liu BL, Fang L, Hu Y, Zhang TZ (2016). Identification and characterization of the GhHsp20 gene family in Gossypium hirsutum. Sci Rep 6, 32517. DOI URL
26	Maere S, de Bodt S, Raes J, Casneuf T, van Montagu M, Kuiper M, van de Peer Y (2005). Modeling gene and genome duplications in eukaryotes. Proc Natl Acad Sci USA 102, 5454-5459. DOI URL
27	Ouyang S, Zhu W, Hamilton J, Lin HN, Campbell M, Childs K, Thibaud-Nissen F, Malek RL, Lee Y, Zheng L, Orvis J, Haas B, Wortman J, Buell CR (2007). The TIGR Rice Genome Annotation Resource: improvements and new features. Nucleic Acids Res 35, D883-D887. DOI URL
28	Park KC, Kim NS (2010). Intron loss mediated structural dynamics and functional differentiation of the polygalacturonase gene family in land plants. Genes Genom 32, 570-577. DOI URL
29	Pertea M, Kim D, Pertea GM, Leek JT, Salzberg SL (2016). Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat Protoc 11, 1650-1667. DOI URL
30	Sarkar NK, Kim YK, Grover A (2009). Rice sHsp genes: genomic organization and expression profiling under stress and development. BMC Genomics 10, 393. DOI URL
31	Scharf KD, Siddique M, Vierling E (2001). The expanding family of Arabidopsis thaliana small heat stress proteins and a new family of proteins containing α-crystallin domains (Acd proteins). Cell Stress Chaperones 6, 225-237. DOI URL
32	Shazadee H, Khan N, Wang JJ, Wang CC, Zeng JG, Huang ZY, Wang XY (2019). Identification and expression profiling of protein phosphatases (PP2C) gene family in Gossypium hirsutum L. Int J Mol Sci 20, 1395. DOI URL
33	Sun WN, Bernard C, Van De Cotte B, Van Montagu M, Verbruggen N (2010). At-HSP17.6A, encoding a small heat-shock protein in Arabidopsis, can enhance osmotolerance upon overexpression. Plant J 27, 407-415. DOI URL
34	The French-Italian Public Consortium for Grapevine Genome Characterization (2007). The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449, 463-467. DOI URL
35	van Montfort RLM, Basha E, Friedrich KL, Slingsby C, Vierling E (2001). Crystal structure and assembly of a eukaryotic small heat shock protein. Nat Struct Biol 8, 1025-1030. PMID
36	Wang L, Zhang SL, Zhang XM, Hu XY, Guo CL, Wang XP, Song JY (2018). Evolutionary and expression analysis of Vitis vinifera OFP gene family. Plant Syst Evol 304, 995-1008. DOI URL
37	Wang WX, Vinocur B, Shoseyov O, Altman A (2004). Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9, 244-252. DOI URL
38	Waters ER, Vierling E (2020). Plant small heat shock proteins—evolutionary and functional diversity. New Phytol 227, 24-37. DOI URL
39	Zhai MZ, Sun YD, Jia CX, Peng SB, Liu ZX, Yang GY (2016). Over-expression of JrsHSP17.3 gene from Juglans regia confer the tolerance to abnormal temperature and NaCl stresses. J Plant Biol 59, 549-558. DOI URL
40	Zhang K, Han YT, Zhao FL, Hu Y, Gao YR, Ma YF, Zheng Y, Wang YJ, Wen YQ (2015). Genome-wide identification and expression analysis of the CDPK gene family in grape, Vitis spp. BMC Plant Biol 15, 164. DOI PMID
41	Zhang LS, Chen F, Zhang XT, Li Z, Zhao YY, Lohaus R, Chang XJ, Dong W, Ho SYW, Liu X, Song AX, Chen JH, Guo WL, Wang ZJ, Zhuang YY, Wang HF, Chen XQ, Hu J, Liu YH, Qin Y, Wang K, Dong SS, Liu Y, Zhang SZ, Yu XX, Wu Q, Wang LS, Yan XQ, Jiao YN, Kong HZ, Zhou XF, Yu CW, Chen YC, Li F, Wang JH, Chen W, Chen XL, Jia QD, Zhang C, Jiang YF, Zhang WB, Liu GH, Fu JY, Chen F, Ma H, van de Peer Y, Tang HB (2020a). The water lily genome and the early evolution of flowering plants. Nature 577, 79-84. DOI URL
42	Zhang LS, Wu SD, Chang XJ, Wang XJ, Zhao YP, Xia YP, Trigiano RN, Jiao YN, Chen F (2020b). The ancient wave of polyploidization events in flowering plants and their facilitated adaptation to environmental stress. Plant Cell Environ 43, 2847-2856. DOI URL
43	Zhang N, Shi JW, Zhao HY, Jiang J (2018). Activation of small heat shock protein (SlHSP17.7) gene by cell wall invertase inhibitor (SlCIF1) gene involved in sugar metabolism in tomato. Gene 679, 90-99. DOI PMID
44	Zhao P, Wang DD, Wang RQ, Kong NN, Zhang C, Yang CH, Wu WT, Ma HL, Chen Q (2018). Genome-wide analysis of the potato Hsp20 gene family: identification, genomic organization and expression profiles in response to heat stress. BMC Genomics 19, 61. DOI URL
45	Zhu W, Lu MH, Gong ZH, Chen RG (2011). Cloning and expression of a small heat shock protein gene CaHSP24 from pepper under abiotic stress. Afr J Biotechnol 10, 4968-4975.
46	Zhu YX, Yan HW, Wang YY, Feng L, Chen Z, Xiang Y (2016). Genome duplication and evolution of heat shock transcription factor (HSF) gene family in four model angiosperms. J Plant Growth Regul 35, 903-920. DOI URL
47	Zhuo XK, Zheng TX, Zhang ZY, Zhang YC, Jiang LB, Ahmad S, Sun LD, Wang J, Cheng TR, Zhang QX (2018). Genome-wide analysis of the NAC transcription factor gene family reveals differential expression patterns and cold-stress responses in the woody plant Prunus mume. Genes (Basel) 9, 494. DOI URL

Protein name	Locus name	Subfamily	Protein length (aa)	Molecular weight (kDa)	Theoretical pI	Instability index	Aliphatic index	GRAVY
NcsHSP01	GWHPAAYW001658	CI	60	6.64	9.16	41.10	99.00	-0.218
NcsHSP02	GWHPAAYW001878	CII	308	34.77	9.03	44.31	74.64	-0.624
NcsHSP03	GWHPAAYW002745	CV	276	30.85	4.88	44.78	77.36	-0.291
NcsHSP04	GWHPAAYW004666	PX	1189	132.46	5.86	44.51	85.53	-0.300
NcsHSP05	GWHPAAYW006130	ER	218	24.32	5.46	64.70	95.14	-0.411
NcsHSP06	GWHPAAYW006158	CII	378	43.02	8.36	50.40	74.76	-0.780
NcsHSP07	GWHPAAYW006159	CII	662	75.02	9.13	55.90	79.64	-0.665
NcsHSP08	GWHPAAYW006161	CII	314	35.79	8.86	47.40	79.39	-0.709
NcsHSP09	GWHPAAYW006746	CIII	164	18.56	5.75	53.09	81.28	-0.489
NcsHSP10	GWHPAAYW007213	CIV	132	14.36	6.83	58.83	82.80	-0.117
NcsHSP11	GWHPAAYW009125	CII	165	19.09	5.48	54.83	69.03	-0.921
NcsHSP12	GWHPAAYW010630	MTII	235	26.36	6.79	56.35	67.57	-0.687
NcsHSP13	GWHPAAYW010715	CI	129	15.42	9.12	60.26	59.53	-1.343
NcsHSP14	GWHPAAYW013759	CVI	154	17.47	5.57	46.32	73.96	-0.573
NcsHSP15	GWHPAAYW014339	CI	156	17.60	5.24	55.71	73.72	-0.552
NcsHSP16	GWHPAAYW014344	CI	158	18.29	8.92	54.19	74.05	-0.682
NcsHSP17	GWHPAAYW015449	MTI/CP	208	23.47	6.01	36.92	78.75	-0.667
NcsHSP18	GWHPAAYW018459	CI	833	94.56	6.14	53.05	69.45	-0.668
NcsHSP19	GWHPAAYW019072	CI	163	18.55	6.19	62.44	71.04	-0.601
NcsHSP20	GWHPAAYW019077	CI	337	37.62	7.83	57.71	78.66	-0.457

Protein name	Locus name	Subfamily	Protein length (aa)	Molecular weight (kDa)	Theoretical pI	Instability index	Aliphatic index	GRAVY
NcsHSP01	GWHPAAYW001658	CI	60	6.64	9.16	41.10	99.00	-0.218
NcsHSP02	GWHPAAYW001878	CII	308	34.77	9.03	44.31	74.64	-0.624
NcsHSP03	GWHPAAYW002745	CV	276	30.85	4.88	44.78	77.36	-0.291
NcsHSP04	GWHPAAYW004666	PX	1189	132.46	5.86	44.51	85.53	-0.300
NcsHSP05	GWHPAAYW006130	ER	218	24.32	5.46	64.70	95.14	-0.411
NcsHSP06	GWHPAAYW006158	CII	378	43.02	8.36	50.40	74.76	-0.780
NcsHSP07	GWHPAAYW006159	CII	662	75.02	9.13	55.90	79.64	-0.665
NcsHSP08	GWHPAAYW006161	CII	314	35.79	8.86	47.40	79.39	-0.709
NcsHSP09	GWHPAAYW006746	CIII	164	18.56	5.75	53.09	81.28	-0.489
NcsHSP10	GWHPAAYW007213	CIV	132	14.36	6.83	58.83	82.80	-0.117
NcsHSP11	GWHPAAYW009125	CII	165	19.09	5.48	54.83	69.03	-0.921
NcsHSP12	GWHPAAYW010630	MTII	235	26.36	6.79	56.35	67.57	-0.687
NcsHSP13	GWHPAAYW010715	CI	129	15.42	9.12	60.26	59.53	-1.343
NcsHSP14	GWHPAAYW013759	CVI	154	17.47	5.57	46.32	73.96	-0.573
NcsHSP15	GWHPAAYW014339	CI	156	17.60	5.24	55.71	73.72	-0.552
NcsHSP16	GWHPAAYW014344	CI	158	18.29	8.92	54.19	74.05	-0.682
NcsHSP17	GWHPAAYW015449	MTI/CP	208	23.47	6.01	36.92	78.75	-0.667
NcsHSP18	GWHPAAYW018459	CI	833	94.56	6.14	53.05	69.45	-0.668
NcsHSP19	GWHPAAYW019072	CI	163	18.55	6.19	62.44	71.04	-0.601
NcsHSP20	GWHPAAYW019077	CI	337	37.62	7.83	57.71	78.66	-0.457

Protein name	Locus name	Subfamily	Protein length (aa)	Molecular weight (kDa)	Theoretical pI	Instability index	Aliphatic index	GRAVY
NcsHSP21	GWHPAAYW019078	CI	156	17.38	5.69	54.61	75.00	-0.449
NcsHSP22	GWHPAAYW019481	CP	222	25.65	9.17	54.03	60.63	-0.880
NcsHSP23	GWHPAAYW022038	CI	159	18.24	5.60	65.94	69.18	-0.648
NcsHSP24	GWHPAAYW025914	CVI	160	18.57	5.82	41.67	70.00	-0.914
NcsHSP25	GWHPAAYW027820	ER	192	21.54	6.54	31.35	102.08	-0.202
NcsHSP26	GWHPAAYW027821	ER	676	74.58	5.31	41.90	85.41	-0.292
NcsHSP27	GWHPAAYW027823	ER	180	20.20	9.21	61.79	73.67	-0.636
NcsHSP28	GWHPAAYW027825	ER	191	21.24	7.93	29.89	91.41	-0.376
NcsHSP29	GWHPAAYW027826	ER	191	21.48	6.00	34.01	98.53	-0.246
NcsHSP30	GWHPAAYW027987	CP	226	25.18	6.65	50.88	75.88	-0.522
NcsHSP31	GWHPAAYW030961	ER	133	15.78	10.21	41.23	77.59	-0.929
NcsHSP32	GWHPAAYW030963	ER	126	14.05	5.63	37.53	109.13	-0.024
NcsHSP33	GWHPAAYW030964	ER	143	15.67	6.08	33.52	109.16	0.075
OssHSP01	LOC_Os01g04340.1	CI	150	16.65	6.31	34.230	77.200	-0.536
OssHSP02	LOC_Os01g04350.1	CI	166	17.89	4.96	55.210	87.590	0.051
OssHSP03	LOC_Os01g04360.1	CI	149	16.90	6.76	47.050	69.870	-0.648
OssHSP04	LOC_Os01g04370.1	CI	150	16.94	6.18	52.240	76.530	-0.605
OssHSP05	LOC_Os01g04380.1	CI	150	16.96	6.18	52.240	73.930	-0.617
OssHSP06	LOC_Os01g08860.1	CII	166	18.03	5.61	45.580	78.130	-0.386
OssHSP07	LOC_Os02g03570.1	CI	177	18.87	6.93	52.450	71.750	-0.406
OssHSP08	LOC_Os02g10710.1	MTII	219	23.59	7.74	47.270	86.030	-0.320
OssHSP09	LOC_Os02g12610.1	CII	175	19.02	5.73	39.010	84.060	-0.486
OssHSP10	LOC_Os02g48140.1	CVII	164	17.77	6.97	46.260	67.320	-0.534
OssHSP11	LOC_Os02g52150.1	MTI/CP	221	24.15	7.96	48.750	77.330	-0.519
OssHSP12	LOC_Os02g54140.1	CIII	172	18.60	7.85	40.550	77.150	-0.538
OssHSP13	LOC_Os03g14180.1	CP	240	26.66	6.78	53.350	75.120	-0.541
OssHSP14	LOC_Os03g15960.1	CI	161	17.91	5.79	57.860	64.780	-0.680
OssHSP15	LOC_Os03g16020.1	CI	154	17.37	6.18	49.280	66.430	-0.706
OssHSP16	LOC_Os03g16030.1	CI	161	18.08	6.77	58.690	61.680	-0.746
OssHSP17	LOC_Os03g16040.1	CI	159	17.66	6.18	55.510	66.790	-0.719
OssHSP18	LOC_Os04g36750.1	ER	215	23.23	5.34	35.060	82.650	-0.365
OssHSP19	LOC_Os05g23140.1	CP	251	27.64	9.42	39.120	69.240	-0.488
OssHSP20	LOC_Os05g42120.1	CV	203	22.28	4.82	54.030	69.800	-0.330
OssHSP21	LOC_Os06g11610.1	MTI/CP	248	26.23	5.27	43.470	79.270	-0.323
OssHSP22	LOC_Os06g14240.1	PX	146	16.02	8.13	36.730	84.790	-0.292
OssHSP23	LOC_Os07g33350.1	CIV	219	23.76	11.74	93.800	71.320	-0.642
OssHSP24	LOC_Os11g13980.1	ER	206	21.87	6.01	48.890	81.500	-0.126
AtsHSP01	AT1G07400.1	CI	157	17.83	5.99	43.380	70.060	-0.680
AtsHSP02	AT1G52560.1	MTII	232	26.54	6.86	45.660	68.880	-0.869
AtsHSP03	AT1G53540.1	CI	157	17.60	5.36	53.800	71.970	-0.578
AtsHSP04	AT1G54050.1	CIII	155	17.36	7.88	58.630	93.680	-0.504
AtsHSP05	AT1G59860.1	CI	155	17.62	6.85	50.240	70.970	-0.678
AtsHSP06	AT2G29500.1	CI	153	17.56	6.33	47.820	71.900	-0.720
AtsHSP07	AT3G46230.1	CI	156	17.44	5.20	46.980	68.590	-0.569

Protein name	Locus name	Subfamily	Protein length (aa)	Molecular weight (kDa)	Theoretical pI	Instability index	Aliphatic index	GRAVY
NcsHSP21	GWHPAAYW019078	CI	156	17.38	5.69	54.61	75.00	-0.449
NcsHSP22	GWHPAAYW019481	CP	222	25.65	9.17	54.03	60.63	-0.880
NcsHSP23	GWHPAAYW022038	CI	159	18.24	5.60	65.94	69.18	-0.648
NcsHSP24	GWHPAAYW025914	CVI	160	18.57	5.82	41.67	70.00	-0.914
NcsHSP25	GWHPAAYW027820	ER	192	21.54	6.54	31.35	102.08	-0.202
NcsHSP26	GWHPAAYW027821	ER	676	74.58	5.31	41.90	85.41	-0.292
NcsHSP27	GWHPAAYW027823	ER	180	20.20	9.21	61.79	73.67	-0.636
NcsHSP28	GWHPAAYW027825	ER	191	21.24	7.93	29.89	91.41	-0.376
NcsHSP29	GWHPAAYW027826	ER	191	21.48	6.00	34.01	98.53	-0.246
NcsHSP30	GWHPAAYW027987	CP	226	25.18	6.65	50.88	75.88	-0.522
NcsHSP31	GWHPAAYW030961	ER	133	15.78	10.21	41.23	77.59	-0.929
NcsHSP32	GWHPAAYW030963	ER	126	14.05	5.63	37.53	109.13	-0.024
NcsHSP33	GWHPAAYW030964	ER	143	15.67	6.08	33.52	109.16	0.075
OssHSP01	LOC_Os01g04340.1	CI	150	16.65	6.31	34.230	77.200	-0.536
OssHSP02	LOC_Os01g04350.1	CI	166	17.89	4.96	55.210	87.590	0.051
OssHSP03	LOC_Os01g04360.1	CI	149	16.90	6.76	47.050	69.870	-0.648
OssHSP04	LOC_Os01g04370.1	CI	150	16.94	6.18	52.240	76.530	-0.605
OssHSP05	LOC_Os01g04380.1	CI	150	16.96	6.18	52.240	73.930	-0.617
OssHSP06	LOC_Os01g08860.1	CII	166	18.03	5.61	45.580	78.130	-0.386
OssHSP07	LOC_Os02g03570.1	CI	177	18.87	6.93	52.450	71.750	-0.406
OssHSP08	LOC_Os02g10710.1	MTII	219	23.59	7.74	47.270	86.030	-0.320
OssHSP09	LOC_Os02g12610.1	CII	175	19.02	5.73	39.010	84.060	-0.486
OssHSP10	LOC_Os02g48140.1	CVII	164	17.77	6.97	46.260	67.320	-0.534
OssHSP11	LOC_Os02g52150.1	MTI/CP	221	24.15	7.96	48.750	77.330	-0.519
OssHSP12	LOC_Os02g54140.1	CIII	172	18.60	7.85	40.550	77.150	-0.538
OssHSP13	LOC_Os03g14180.1	CP	240	26.66	6.78	53.350	75.120	-0.541
OssHSP14	LOC_Os03g15960.1	CI	161	17.91	5.79	57.860	64.780	-0.680
OssHSP15	LOC_Os03g16020.1	CI	154	17.37	6.18	49.280	66.430	-0.706
OssHSP16	LOC_Os03g16030.1	CI	161	18.08	6.77	58.690	61.680	-0.746
OssHSP17	LOC_Os03g16040.1	CI	159	17.66	6.18	55.510	66.790	-0.719
OssHSP18	LOC_Os04g36750.1	ER	215	23.23	5.34	35.060	82.650	-0.365
OssHSP19	LOC_Os05g23140.1	CP	251	27.64	9.42	39.120	69.240	-0.488
OssHSP20	LOC_Os05g42120.1	CV	203	22.28	4.82	54.030	69.800	-0.330
OssHSP21	LOC_Os06g11610.1	MTI/CP	248	26.23	5.27	43.470	79.270	-0.323
OssHSP22	LOC_Os06g14240.1	PX	146	16.02	8.13	36.730	84.790	-0.292
OssHSP23	LOC_Os07g33350.1	CIV	219	23.76	11.74	93.800	71.320	-0.642
OssHSP24	LOC_Os11g13980.1	ER	206	21.87	6.01	48.890	81.500	-0.126
AtsHSP01	AT1G07400.1	CI	157	17.83	5.99	43.380	70.060	-0.680
AtsHSP02	AT1G52560.1	MTII	232	26.54	6.86	45.660	68.880	-0.869
AtsHSP03	AT1G53540.1	CI	157	17.60	5.36	53.800	71.970	-0.578
AtsHSP04	AT1G54050.1	CIII	155	17.36	7.88	58.630	93.680	-0.504
AtsHSP05	AT1G59860.1	CI	155	17.62	6.85	50.240	70.970	-0.678
AtsHSP06	AT2G29500.1	CI	153	17.56	6.33	47.820	71.900	-0.720
AtsHSP07	AT3G46230.1	CI	156	17.44	5.20	46.980	68.590	-0.569

Protein name	Locus name	Subfamily	Protein length (aa)	Molecular weight (kDa)	Theoretical pI	Instability index	Aliphatic index	GRAVY
AtsHSP08	AT4G10250.1	ER	195	22.00	5.58	36.450	93.950	-0.469
AtsHSP09	AT4G21870.1	CIV	134	15.39	5.17	73.930	93.810	-0.325
AtsHSP10	AT4G25200.1	MTI/CP	210	23.61	6.46	58.790	80.760	-0.649
AtsHSP11	AT4G27670.1	CP	227	25.34	8.49	46.860	72.070	-0.641
AtsHSP12	AT5G12020.1	CII	155	17.62	6.32	38.840	80.390	-0.617
AtsHSP13	AT5G12030.1	CII	156	17.69	5.59	44.370	75.000	-0.596
AtsHSP14	AT5G37670.1	PX	137	15.70	7.94	50.680	86.640	-0.512
AtsHSP15	AT5G51440.1	MTI/CP	210	23.47	8.96	52.510	84.000	-0.558
AtsHSP16	AT5G54660.1	CV	192	21.66	5.47	38.030	71.560	-0.500
AtsHSP17	AT5G59720.1	CI	161	18.13	6.77	48.090	67.200	-0.657
VvsHSP01	VIT_200s0707g00010.1	CIV	136	15.69	4.89	53.490	82.430	-0.315
VvsHSP02	VIT_200s0992g00020.1	CIV	136	15.70	5.01	54.190	82.430	-0.312
VvsHSP03	VIT_201s0010g02290.1	CP	226	25.56	6.77	48.710	62.170	-0.706
VvsHSP04	VIT_202s0154g00480.1	MTI/CP	201	22.45	9.24	45.150	77.060	-0.531
VvsHSP05	VIT_202s0154g00490.1	MTI/CP	201	22.55	9.11	51.710	75.670	-0.561
VvsHSP06	VIT_204s0008g01490.1	CII	156	17.34	5.94	41.520	82.500	-0.444
VvsHSP07	VIT_204s0008g01500.1	CII	152	16.69	6.84	42.090	79.540	-0.390
VvsHSP08	VIT_204s0008g01510.1	CII	156	17.40	5.77	44.190	76.220	-0.462
VvsHSP09	VIT_204s0008g01520.1	CII	156	17.58	5.58	40.180	78.080	-0.513
VvsHSP10	VIT_204s0008g01530.1	CII	480	53.16	8.89	39.780	68.600	-0.713
VvsHSP11	VIT_204s0008g01550.1	CII	156	17.41	5.94	39.580	71.790	-0.533
VvsHSP12	VIT_204s0008g01560.1	CII	113	12.66	8.66	38.840	83.540	-0.473
VvsHSP13	VIT_204s0008g01570.1	CII	166	18.60	5.95	40.640	68.670	-0.542
VvsHSP14	VIT_204s0008g01580.1	CII	156	17.42	6.62	42.220	76.790	-0.510
VvsHSP15	VIT_204s0008g01590.1	CII	155	17.29	5.94	37.610	81.030	-0.466
VvsHSP16	VIT_204s0008g01610.1	CII	158	18.14	6.33	40.180	75.820	-0.617
VvsHSP17	VIT_204s0008g01620.1	CII	159	18.42	8.46	42.080	83.900	-0.459
VvsHSP18	VIT_206s0004g05770.1	CI	144	16.31	6.93	33.000	75.070	-0.642
VvsHSP19	VIT_208s0058g00210.1	CI	148	16.88	5.81	64.560	66.490	-0.629
VvsHSP20	VIT_209s0002g00640.1	CIII	160	17.89	6.30	49.690	81.000	-0.516
VvsHSP21	VIT_209s0002g06790.1	MTII	233	26.31	7.78	53.870	82.060	-0.750
VvsHSP22	VIT_212s0035g01910.1	ER	250	28.39	7.94	49.940	89.400	-0.388
VvsHSP23	VIT_213s0019g00860.1	PX	142	15.81	6.75	51.850	85.000	-0.311
VvsHSP24	VIT_213s0019g02740.1	CI	151	17.17	5.81	46.350	74.110	-0.553
VvsHSP25	VIT_213s0019g02760.1	CI	140	15.80	6.77	42.530	72.290	-0.589
VvsHSP26	VIT_213s0019g02770.1	CI	151	17.10	5.81	48.460	72.850	-0.554
VvsHSP27	VIT_213s0019g02780.1	CI	151	17.02	5.80	45.690	70.260	-0.587
VvsHSP28	VIT_213s0019g02820.1	CI	151	17.12	5.81	47.080	70.260	-0.591
VvsHSP29	VIT_213s0019g02840.1	CI	151	17.09	5.54	50.220	72.850	-0.551
VvsHSP30	VIT_213s0019g02850.1	CI	151	17.05	5.80	45.440	70.260	-0.590
VvsHSP31	VIT_213s0019g02900.1	CI	108	12.64	6.18	52.990	80.190	-0.798
VvsHSP32	VIT_213s0019g02920.1	CI	136	15.27	5.70	46.020	79.490	-0.552
VvsHSP33	VIT_213s0019g02930.1	CI	160	18.17	6.78	53.430	76.690	-0.644
VvsHSP34	VIT_213s0019g03000.1	CI	160	18.15	7.93	55.700	76.690	-0.644