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Research Article

Grafting-Induced Gene Expression Change in Brassica rapa Leaves is Different from Fruit Trees

Myeong-il Mun1, Hankuil Yi1, Ill-Sup Nou2, Yoonkang Hur1,*
Plant Breeding and Biotechnology 2015;3(1):67-76.
Published online: March 31, 2015

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*Corresponding author: Yoonkang Hur, ykhur@cnu.ac.kr, Tel: +82-42-821-6279, Fax: +82-42-822-9690
• Received: March 20, 2015   • Revised: March 23, 2015   • Accepted: March 23, 2015

Copyright © 2015 The Korean Society of Breeding Science

This is an Open-Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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  • Grafting has widely used in the agriculture of fruit-bearing crops and trees because rootstocks have a profound influence on many aspects of scion development and scion responses to the environmental changes including biotic and abiotic stress tolerance. These effects appear to result from the change of gene expression on scion, but only limited numbers of papers have been published demonstrating it. To identify altered expression of genes in Chinese cabbage, Chiifu(Brassica rapa ssp. pekinensis, inbred line) shoot was grafted on three Brassica rootstocks: mustard, turnip and broccoli. After head formation, Br300K microarray experiment was conducted using total RNAs from scion leaves collected in two different seasons, spring (June) and fall (October). A large number of differentially expressed genes (DEGs) were identified both in two seasonal samples, but DEGs were more notable in June sample than in October sample. However, the number of DEGs by three rootstocks were high in October with respect to up-regulation, but high in June for down-regulation. Categories of DEGs included metal ion binding, response to hormonal stimuli, response to endogenous stimuli, regulation of transcription, oxidation reduction and response to stress. Up-regulated genes in both June and October samples were similar in mustard and turnip rootstocks, but different in broccoli rootstock. Two genes were found to respond to all experimental conditions: Brapa_ESTC049008 (hypothetical protein) as an up-regulated gene and Brapa_ESTC016027 (CNGC12) as a down-regulated gene. Together with the previous reports, these results suggest that grafting-induced gene expression depends on the species involved.
  • Key words: Microarray, Chiifu, heterografting, MBP2, CNGC12
Grafting has widely used in the agriculture of fruit-bearing crops because rootstocks are known to provide scion biomass and quality as well as biotic and abiotic stress tolerance (Lee 1994, 2003; Cleaswater et al. 2006; Kubota and McClure 2008; Lee et al. 2010; Gregory et al. 2013; Koepke and Dhingra 2013). Grafting also affects pH, fragrance, color, sugar and carotenoid contents, and texture in fruits of Cucurbits and tomatoes (Davis et al. 2008). As a result, most grafting studies have focused on Cucurbits, tomato, grape and fruit trees, with little attention to the vegetables.
Since grafting connects vascular tissues between rootstocks and scions, various substances can be exchanged. Among others, minerals, amino acids, carboxylic acids, ions, phenylpropanoids and hormones could be transported from rootstocks to scions by xylem sap (Gollan et al. 1992; Goodger et al. 2005; Alvarez et al. 2008; Wu et al. 2009). In addition, various proteases are also transported through xylem sap (Biles and Abeles 1991; Satoh et al. 1992; Bhutz et al. 2004; Kehr et al. 2005; Alvarez et al. 2006). Various materials could also be transported through phloem by grafting (Le Hir et al. 2008): carbohydrate, amino acids, hormones and mRNAs (Ruiz-Medrano et al. 1999; Wu et al. 2002; Banerjee et al. 2006; Lough and Lucas 2006; Kehr and buhtz 2008), small RNA (Yoo et al. 2004; Pant et al. 2008), and proteins (Corbesier et al. 2007; Lin et al. 2007; Weller et al. 2009).
It was suggested that many developmental phenomena induced by grafting are caused by long-distance transmissible substances via phloem and xylem: flowering (Zeevaart 1976; Lang et al. 1977), tuber formation (Jackson 1999), nodule formation (Oka-Kira and Kawaguchi 2006), leaf development (Kim et al. 2001), lateral shoot formation (Beveridge 2006) and defense (Palauqui et al. 1997). Recent articles demonstrate that flowering is associated with long-distance transmissible substances, such as CONSTANS mRNA (Ayre and Turgeon 2004), FT mRNA (Huang et al. 2005), FT protein (Corbesier et al. 2007; Lin et al. 2007), and GIGANTEA and ELF4 proteins (Weller et al. 2009). FT and siRNAs in phloem, which lead epigenetic regulation, can be applied in crop breeding (McGarry and Kragler 2013).
A few reports have reported scion gene expression change upon grafting (Jensen et al. 2003, 2010; Prassinos et al. 2009; Cookson and Ollat 2013). It was showing that several categories of genes are differentially expressed in genetically identical apple scions, when grafted on rootstocks with different genotypes. Differentially expressed genes (DEGs) include those responding stimulus and abiotic and biotic stress, in addition to genes with unknown biological processes and other biological processes (Jensen et al. 2010). Prassinos et al. (2009) used cDNA amplified fragment length polymorphism to compare the effect of a dwarfing and a semi-vigorous rootstocks on gene expression in the scion and observed the differential regulation of various transcription factors and genes involved in signaling processes. In addition, Cookson and Ollat (2013) demonstrated that heterografts induce more stress-responsive genes than autografts in grapevines.
Genus Brassica belongs to the mustard family (Brassicaceae) showing various morphology and includes B. rapa, B. nigra, B. oleracea, B. juncea, B. napus and B. carinata, which are important edible crops across the world. Brasscia plants include many important vegetable crops contain very potent phytochemicals: cabbage, kale, Brussels sprouts, cauliflower, broccoli, and kohlrabi, with glucosinolates, and their breakdown products (Mithen et al. 2000; Park et al. 2012). Chinese cabbage (B. rapa ssp. pekinensis) is one of the most important leafy vegetables widely used in East Asian countries. To examine the change in gene expression by grafting, we have used Chiifu inbred line (B. rapa ssp. pekinensis) as scion and various rootsocks, such as Chiifu (grafting control), turnip (B. rapa ssp. rapa), mustard (B. juncea) and broccoli (B. oleracea). When comparing homo-and heterografting results, we found a larger number of genes in the leaves of scion (Chiifu leaves) are differentially expressed by hetero-grafting.
Plant materials
Chiifu inbred line (B. rapa ssp. pekinensis) used as scion was obtained from Korea Brassica rapa Genome Resource Bank (KBGRB) and various rootsocks’ seeds, such as turnip (B. rapa ssp. rapa), mustard (B. juncea) and broccoli (B. oleracea Italica), were purchased from local market in Korea. Seeds were sown in 50-hole pot and grown in a greenhouse for 2 weeks until the first foliage leaf was emerged. Grafting was performed with Y-type and resulting plants were put into a growth room with controlled moisture over 90%. After acclimation, grafted-seedlings were transplanted to soil and grown for 2 months until heads were formed. Leaf tissues from outer and inner leaves of scion were sampled from 5 independent plants in June 4 for spring and October 29 for fall growing plants, and frozen immediately in liquid nitrogen.
RNA extraction and microarray
Total RNAs were extracted after combining outer and inner leaves of scion using TriZol reagent (Invitrogen, USA) and further purified using an RNeasy MinElute™ Cleanup Kit (Quagen, Germany). For microarray experiment, 300k microarray chip (Version 2.0) for B. rapa, which was designed from 47,548 unigenes and manufactured by NimbleGen, Inc. (http://www.nimblegen.com/) were used (Dong et al. 2013). To assess the reproducibility of the microarray analysis, we repeated the experiment two times using independently prepared total RNA. The data were then normalized and processed with cubic spline normalization using quantile to adjust signal variations between chips and robust multichip analysis using a median polish algorithm implemented in NimbleScan (Workman et al. 2002; Irizarry et al. 2003). RNA preparation, GeneChip hybridization, and data analyses were conducted as previously described (Dong et al. 2013).
Gene chip data analysis
Genes with adjusted p-value or false discovery rate below 0.05 were collected and further selected for those with expression difference greater than or less than at least one treatment. Multivariate statistical tests such as principal component analysis, and multidimensional scaling were performed with Acuity 3.1 (Molecular Devices, U.S.A.). Clustering analysis was carried out with MultiExperiment Viewer version 4.9 (MeV4.9, http://www.tm4.org/mev.html). To gain the insight on putative biological functions and biochemical pathways of DEGs, we carried out enrichment analyses by searching the Gene Ontology (GO) (Ashburner et al. 2000) and agriGO (Du et al. 2010).
Grafted Chinese cabbage
Rootstocks widely used in agriculture can have a profound influence on many aspects of scion development and scion responses to the environment (Webster 2004; Lee et al. 2010; Gregory et al. 2013). These influences might be related to the change in gene expression by transmissible substances through phloem (Sonoda and Nishiguchi 2000; Huang et al. 2005; Kehr and Buhtz 2008; Notaguchi et al. 2008; McGarry and Kragler 2013) and xylem (Ko et al. 2014). Therefore, gene expression in scion can be influenced by both root and shoot parts of rootstocks. To examine the gene expression upon grafting, we used Chiifu inbred line as scion and three Brassica species as rootstocks. Grafted-Chinese cabbages were grown in two seasons, spring (April 1 to June 4) and fall (Aug. 10 to Oct. 29). Temperature ranges during 7 days before sampling were 13.9°C (low) - 24.7°C (high) for spring and 8.6°C (low) - 18.0°C (high) for fall. To eliminate temperature and rootstock biases, fold change in gene expression was calculated based on homografting (or autografting) values (Chiifu sicon vs. Chiifu rootstock) (Fig. 1 and Table S1). As shown in Figure 1, shoot for each rootstock remained so that gene expression in Chiifu scion can be affected by mobile substances from both xylem and phloem of rootstocks. Rootstock without the shoot parts showed much less effect on scion gene expression change (data not shown).
Microarray data analysis to identify DEGs
Contrast to horticultural point of view on grafting, which aims to increase the biomass and stress tolerance of scion, our experiment was conducted to examine the changes at the gene expression level, by using different rootstocks (Table S1). Hetero-grafted Chiifu scion with three different rootstocks resulted in the differential expression of a large number of genes in the scion leaves, when compared to the auto-grafted control Chiifu/Chiifu (Fig. 2). The number of DEGs was dependent on season when Chinese cabbages were grown: more genes were up- and down-regulated in the June sample compared to the October one. This might be due to high light intensity and temperature in June. Regarding to rootstocks, the differential expression of most genes was similar in mustard and turnip, but rather different in broccoli. The number of DEGs shared by all three rootstocks used was higher in October (74 vs. 35) with respect to up-regulation, but higher in June for down-regulation (88 vs. 25) (Fig. 2). When these genes were further analyzed by functional category, most genes belonged to the categories of metal ion binding, response to hormonal stimuli, response to endogenous stimuli, regulation of transcription, oxidation reduction and response to stress (Table 1). Interestingly, genes involved in metal ion binding and response to hormonal stimuli occupied the first and second places.
Alteration of gene expression by grafting has been examined in apple trees (Prassinos et al. 2009; Jensen et al. 2010) and grape vines (Cookson and Ollat 2013). In both plants, autografting did not induce shoot gene expression, but heterografting had great effect on gene expression. However, functional category or Gene Ontology (GO) terms were different between two species. In apple trees, GO terms enriched in the differentially expressed genes were response to stimulus, response to abiotic and biotic stress, among others. (Jensen et al. 2010). In addition, the authors identified 116 genes, whose expression levels were correlated with the plant size. Using a dwarfing and a semi-vigorous rootstocks, Prassinos et al. (2009) identified differential regulation for many transcription factors and genes involved in signaling processes using scion shoot apex. In grape grafting, categories of genes showing increased expression at shoot apex were genes related to DNA, chromatin structure, histones, flavonoids, and leucine rich repeat containing receptor kinases (Cookson and Ollat 2013). These results suggest that grafting-induced gene expression change is species-specific, except developmentally determined genes like those involved in FT-induced flowering.
Identification of genes showing rootstock-dependent responses
To identify DEGs whose expression is regulated in rootstock-dependent manners regardless of growth conditions, commonly up- or down-regulated genes in both June and October samples were analyzed (Fig. 3). Similar numbers of genes were differentially regulated when mustard and turnip were used as rootstocks, but broccoli-grafted scions showed different pattern compared to the other two species. Regarding up-regulated genes, samples obtained using mustard and turnip rootstocks shared many genes, quite different from that obtained using broccoli rootstock (Table 2). The most notable genes were myrosinase-binding protein 2 (MBP2) and unknown protein genes. MBP2 has been known to form a complex with myrosinase, which degrades secondary metabolites, glucosinolates, upon wounding to provide a defense mechanism against pests. Binding of MBP2 prevents degradation of the complex, but its exact function is still unclear (Erisson et al. 2002). It is also not known why the expression of MBP2 is dramatically increased upon grafting in Chinese cabbage. In scions grafted to mustard and turnip rootstock, carbonic anhydrase (CA) gene, which regulates CO2-controlled stomatal movement in guard cells, was also up-regulated (Table S1 and Table 1). Interestingly, up-regulated genes identified with broccoli rootstock included floral bud specific genes, such as ASK-beta (ASK2) and ANAC025 (Dong et al. 2013). In addition, various CYP genes were also up-regulated when broccoli rootstock were used. Another interesting finding was anthocyanin biosynthesis-related genes were induced as a result of grafting with the rootstock of mustard (flavonol synthase, FLS and chalcone synthase, CHS) and turnip (FLS), but not with that of broccoli. Down-regulated genes were variable depending on the species used for rootstocks, except cyclic nucleotide gated channel 12 (CNGC12) which was down-regulated in all three combinations.
Only two genes were commonly regulated in three rootstocks: Brapa_ESTC049008 (hypothetical protein) for up-regulation and Brapa_ESTC016027 (CNGC12) for down-regulation (Table 3, Fig. 3). Brapa_ESTC049008 consists of 76 bp of 5′-UTR, 192 bp coding sequences (CDS) and 291 bp long 3′-UTR. Its CDS encodes 7 kDa hypothetical proteins with pI 8.0. Brapa_ESTC049008 is 75% identical to Arabidopsis protein (AT1G49500) at the amino acid sequence level. Brapa_ESTC016027 encodes Brassica homolog of cyclic nucleotide gated channel 12 (CNGC12, which is a positive regulator of resistance against avirulent fungal pathogen (Yoshioka et al. 2006; Urquhart et al. 2011). It is intriguing why grafting down-regulates CNGC12 gene, which leads to the increase in calcium sensitivity.
Recent works have focused on the mechanisms of tissue reunion during grafting, such as exchange of genetic materials in various plants (Stegemann and Bock 2009; Asahina and Satoh 2015). Although only limited numbers of papers have been reported for scion gene expression change by grafting, it was revealed that heterografts induce more stress-responsive genes than autografts (Cookson et al. 2014). Our results are different from previous reports since rootstocks and scions from two related vegetable species were used. To learn more about the influence of grafting on scion gene expression, gene expression needs to be examined at various growth and developmental stages.
Grafting Chiifu inbred line with rootstocks originating from various Brassica spp. had a profound effect on scion gene expression changes, when tested in two different seasons of a year. In contrast to the grafting for fruit production using vigorous rootstocks, our grafting experiment was to identify gene expression changes induced by substances from both rootstock and rootstock-bearing shoot (i.e., xylem and phloem). DEGs were more notable in June sample than in October sample. However, the number of DEGs identified by the use of three different rootstocks was higher in the samples collected in October for up-regulation, while the number was higher in June sample for down-regulation. DEGs identified includes the genes categorized for metal ion binding, response to hormonal stimuli, response to endogenous stimuli, regulation of transcription, oxidation reduction and response to stress. Up-regulated genes in both June and October samples were found similar between scions on mustard and turnip rootstocks, but somewhat different in that on broccoli rootstock. In contrast, no patterns were observed for down-regulated genes. Two genes were identified in all three experimental set-ups: Brapa_ESTC049008 (hypothetical protein) as an up-regulated gene and Brapa_ESTC016027 (CNGC12) as a down-regulated genes. Functional analysis of several genes identified in this study, using transgenic and biochemical approaches, will be necessary to further understand molecular changes induced by grafting and improve the productivity.
Supplementary Table 1
Result of Br300K microarray. Microarray was performed with scion tissues on different rootstocks. PI values represent prove intensity of hybridization. Yellow and blue shades indicate over two-fold change in PI values.
PBB-03-67-suppl.pdf
This work was supported by Research Fund of Chungnam National University (CNU), Daejeon, Korea, to Yoonkang Hur (2014-0905-01).
Fig. 1
Morphology of grafted-Chinese cabbages: overall appearance (upper panels) and longitudinal section (bottom). Arrows indicate sampled tissues (outer and inner leaves) for microarray. Grafting control was Chiifu (scion)/Chiifu (rootstock). Note that rootstock and scion of the grafting control was separated before photography.
pbb-03-67f1.jpg
Fig. 2
Venn diagram showing differentially expressed genes (DEGs) by three rootstocks compared to homografting. A and B represent up-regulated genes in June and October samples, respectively. C and D represent down-regulated genes in June and October samples, respectively.
pbb-03-67f2.jpg
Fig. 3
Venn diagrams showing differentially expressed genes (DEGs) in both June and October experiments by three different rootstocks, compared to homografting. A and B represent up-regulated and down-regulated genes, respectively.
pbb-03-67f3.jpg
Table 1
Functional categorization of DEGs by different rootstocks.
Table 1
Functional category Up-regulated Down-regulated
June Oct. June Oct.
Metal ion binding 9 23 24 8
Response to hormone stimulus 7 15 2 4
Response to endogenous stimulus 3 10 2 3
Regulation of transcription 9 6 8 1
Oxidation reduction 4 4 7 6
Response to stress 6 2 3 4
Transferase 4 2 4 10
Membrane 2 13 1 6
Response to inorganic substance 3 1 4 4
Chloroplast 0 15 2 6
Hydrolase 0 3 6 1
Monooxygenase 1 3 3 0
Signal peptide 0 6 7 3
Glycoprotein 0 3 6 2
Heat shock protein binding 3 0 1 0
Response to inorganic substance 3 1 4 4
Response to cadmium ion 2 1 0 0
Lipid transport 0 4 1 1
Lipid degradation 0 2 1 1
Response to nutrient level 1 1 1 0
Cellular response to stress 1 1 2 4
Reproductive developmental process 1 6 3 0
Table 2
Top 5 genes that were commonly regulated in both June and October samples.
Table 2
Expression Rootstock Br_SEQ_ID At Locus Description PI value Fold change
Chiifu Rootstock Rootstock/Chiifu
June Oct June Oct June Oct
Up-regulation Mustard Brapa_ESTC016277 AT1G52030 MBP2 (MYROSINASE-BINDING PROTEIN 2) 470 413 5,099 2,022 10.9 4.9
Brapa_ESTC007567 AT1G52030 MBP2 (MYROSINASE-BINDING PROTEIN 2) 479 345 4,090 1,893 8.5 5.5
Brapa_ESTC010078 AT4G27360 Dynein light chain, putative 11 19 56 138 5.3 7.4
Brapa_ESTC013929 AT3G01500 CA1 (CARBONIC ANHYDRASE 1) 1460 319 4450 2079 3.0 6.5
Brapa_ESTC000600 AT1G16850 Unknown protein 376 1,063 3,532 4,888 9.4 4.6
Turnip Brapa_ESTC007567 AT1G52030 MBP2 (MYROSINASE-BINDING PROTEIN 2) 479 345 8,002 2,570 16.7 7.5
Brapa_ESTC016277 AT1G52030 MBP2 (MYROSINASE-BINDING PROTEIN 2) 470 413 8,909 2,364 19.0 5.7
Brapa_ESTC049008 AT1G49500 Unknown protein 15 28 449 154 29.6 5.4
Brapa_ESTC026374 AT5G59310 LTP4 (LIPID TRANSFER PROTEIN 4) 3,006 282 11,584 3,312 3.9 11.7
Brapa_ESTC022106 AT3G01500 CA1 (CARBONIC ANHYDRASE 1) 5,941 532 20,763 5,420 3.5 10.2
Broccoli Brapa_ESTC008104 AT3G49620 DIN11 (DARK INDUCIBLE 11); oxidoreductase 605 106 4,580 645 7.6 6.1
Brapa_ESTC049008 AT1G49500 Unknown protein 15 28 106 162 7.0 5.7
Brapa_ESTC026957 AT3G49620 DIN11 (DARK INDUCIBLE 11); oxidoreductase 1,151 347 4,544 1,435 3.9 4.1
Brapa_ESTC047756 AT3G51590 LTP12 (LIPID TRANSFER PROTEIN 12) 322 209 831 632 2.6 3.0
Brapa_ESTC028727 AT3G15400 ATA20 (Arabidopsis thaliana anther 20) 150 139 327 586 2.2 4.2
Down-regulation Mustard Brapa_ESTC016027 AT2G46450 ATCNGC12 (cyclic nucleotide gated channel 12) 707 70 101 11 −7.0 −6.1
Brapa_ESTC022776 AT1G06160 Ethylene-responsive factor, putative 4,299 466 962 71 −4.5 −6.5
Brapa_ESTC044452 AT4G23990 ATCSLG3 (Cellulose synthase-like G3) 1,958 1,605 477 279 −4.1 −5.8
Brapa_ESTC022540 AT5G20820 Auxin-responsive protein-related 400 474 40 232 −9.9 −2.0
Brapa_ESTC014184 AT5G49360 BXL1 (BETA-XYLOSIDASE 1) 847 141 314 34 −2.7 −4.1
Turnip Brapa_ESTC026136 AT3G01420 ALPHA-DOX1 (ALPHA-DIOXYGENASE 1) 3,059 2,016 287 204 −10.7 −9.9
Brapa_ESTC016027 AT2G46450 ATCNGC12 (cyclic nucleotide gated channel 12) 707 70 15 15 −46.8 −4.5
Brapa_ESTC006382 AT5G45340 CYP707A3 (cytochrome P450, family 707, subfamily A, polypeptide 3) 4,649 906 962 220 −4.8 −4.1
Brapa_ESTC004877 no_hits_found --------- 315 161 100 40 −3.2 −4.0
Brapa_ESTC012086 AT4G16260 Glycosyl hydrolase family 17 protein 7,703 764 523 272 −14.7 −2.8
Broccoli Brapa_ESTC014184 AT5G49360 BXL1 (BETA-XYLOSIDASE 1); hydrolase, hydrolyzing O-glycosyl compounds 847 141 34 18 −25.1 −7.9
Brapa_ESTC002586 AT4G35770 DIN1 | SEN1 (DARK INDUCIBLE 1) 6,771 562 22 135 −303.4 −4.2
Brapa_ESTC016027 AT2G46450 CNGC12, ATCNGC12 | ATCNGC12 (cyclic nucleotide gated channel 12) 707 70 7 12 −106.0 −5.9
Brapa_ESTC021555 AT4G15530 PPDK (PYRUVATE ORTHOPHOSPHATE DIKINASE) 4,100 604 310 100 −13.2 −6.1
Brapa_ESTC007363 AT4G37010 Calcium ion binding 1,109 145 77 26 −14.4 −5.5
Table 3
Genes that are differentially expressed in all experimental samples as well as both June and October samples.
Table 3
Br_SEQ_ID At Locus Description Fold change
Mustard/Chiifu Turnip/Chiifu Broccoli/Chiifu
June Oct. June Oct. June Oct.
Brapa_ESTC049008 AT1G49500 Hypothetical protein 34.5 3.0 29.6 5.4 7.0 5.7
Brapa_ESTC016027 AT2G46450 CNGC12 −7.0 −6.1 −46.8 −4.5 −106.0 −5.9
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Grafting-Induced Gene Expression Change in Brassica rapa Leaves is Different from Fruit Trees
Plant Breed. Biotech.. 2015;3(1):67-76.   Published online March 31, 2015
DOI: https://doi.org/10.9787/PBB.2015.3.1.067
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Grafting-Induced Gene Expression Change in Brassica rapa Leaves is Different from Fruit Trees
Plant Breed. Biotech.. 2015;3(1):67-76.   Published online March 31, 2015
DOI: https://doi.org/10.9787/PBB.2015.3.1.067
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Grafting-Induced Gene Expression Change in Brassica rapa Leaves is Different from Fruit Trees
Image Image Image
Fig. 1 Morphology of grafted-Chinese cabbages: overall appearance (upper panels) and longitudinal section (bottom). Arrows indicate sampled tissues (outer and inner leaves) for microarray. Grafting control was Chiifu (scion)/Chiifu (rootstock). Note that rootstock and scion of the grafting control was separated before photography.
Fig. 2 Venn diagram showing differentially expressed genes (DEGs) by three rootstocks compared to homografting. A and B represent up-regulated genes in June and October samples, respectively. C and D represent down-regulated genes in June and October samples, respectively.
Fig. 3 Venn diagrams showing differentially expressed genes (DEGs) in both June and October experiments by three different rootstocks, compared to homografting. A and B represent up-regulated and down-regulated genes, respectively.

Fig. 1

Fig. 2

Fig. 3

Grafting-Induced Gene Expression Change in Brassica rapa Leaves is Different from Fruit Trees

Functional categorization of DEGs by different rootstocks.

Functional category Up-regulated Down-regulated
June Oct. June Oct.
Metal ion binding 9 23 24 8
Response to hormone stimulus 7 15 2 4
Response to endogenous stimulus 3 10 2 3
Regulation of transcription 9 6 8 1
Oxidation reduction 4 4 7 6
Response to stress 6 2 3 4
Transferase 4 2 4 10
Membrane 2 13 1 6
Response to inorganic substance 3 1 4 4
Chloroplast 0 15 2 6
Hydrolase 0 3 6 1
Monooxygenase 1 3 3 0
Signal peptide 0 6 7 3
Glycoprotein 0 3 6 2
Heat shock protein binding 3 0 1 0
Response to inorganic substance 3 1 4 4
Response to cadmium ion 2 1 0 0
Lipid transport 0 4 1 1
Lipid degradation 0 2 1 1
Response to nutrient level 1 1 1 0
Cellular response to stress 1 1 2 4
Reproductive developmental process 1 6 3 0

Top 5 genes that were commonly regulated in both June and October samples.

Expression Rootstock Br_SEQ_ID At Locus Description PI value Fold change
Chiifu Rootstock Rootstock/Chiifu
June Oct June Oct June Oct
Up-regulation Mustard Brapa_ESTC016277 AT1G52030 MBP2 (MYROSINASE-BINDING PROTEIN 2) 470 413 5,099 2,022 10.9 4.9
Brapa_ESTC007567 AT1G52030 MBP2 (MYROSINASE-BINDING PROTEIN 2) 479 345 4,090 1,893 8.5 5.5
Brapa_ESTC010078 AT4G27360 Dynein light chain, putative 11 19 56 138 5.3 7.4
Brapa_ESTC013929 AT3G01500 CA1 (CARBONIC ANHYDRASE 1) 1460 319 4450 2079 3.0 6.5
Brapa_ESTC000600 AT1G16850 Unknown protein 376 1,063 3,532 4,888 9.4 4.6
Turnip Brapa_ESTC007567 AT1G52030 MBP2 (MYROSINASE-BINDING PROTEIN 2) 479 345 8,002 2,570 16.7 7.5
Brapa_ESTC016277 AT1G52030 MBP2 (MYROSINASE-BINDING PROTEIN 2) 470 413 8,909 2,364 19.0 5.7
Brapa_ESTC049008 AT1G49500 Unknown protein 15 28 449 154 29.6 5.4
Brapa_ESTC026374 AT5G59310 LTP4 (LIPID TRANSFER PROTEIN 4) 3,006 282 11,584 3,312 3.9 11.7
Brapa_ESTC022106 AT3G01500 CA1 (CARBONIC ANHYDRASE 1) 5,941 532 20,763 5,420 3.5 10.2
Broccoli Brapa_ESTC008104 AT3G49620 DIN11 (DARK INDUCIBLE 11); oxidoreductase 605 106 4,580 645 7.6 6.1
Brapa_ESTC049008 AT1G49500 Unknown protein 15 28 106 162 7.0 5.7
Brapa_ESTC026957 AT3G49620 DIN11 (DARK INDUCIBLE 11); oxidoreductase 1,151 347 4,544 1,435 3.9 4.1
Brapa_ESTC047756 AT3G51590 LTP12 (LIPID TRANSFER PROTEIN 12) 322 209 831 632 2.6 3.0
Brapa_ESTC028727 AT3G15400 ATA20 (Arabidopsis thaliana anther 20) 150 139 327 586 2.2 4.2
Down-regulation Mustard Brapa_ESTC016027 AT2G46450 ATCNGC12 (cyclic nucleotide gated channel 12) 707 70 101 11 −7.0 −6.1
Brapa_ESTC022776 AT1G06160 Ethylene-responsive factor, putative 4,299 466 962 71 −4.5 −6.5
Brapa_ESTC044452 AT4G23990 ATCSLG3 (Cellulose synthase-like G3) 1,958 1,605 477 279 −4.1 −5.8
Brapa_ESTC022540 AT5G20820 Auxin-responsive protein-related 400 474 40 232 −9.9 −2.0
Brapa_ESTC014184 AT5G49360 BXL1 (BETA-XYLOSIDASE 1) 847 141 314 34 −2.7 −4.1
Turnip Brapa_ESTC026136 AT3G01420 ALPHA-DOX1 (ALPHA-DIOXYGENASE 1) 3,059 2,016 287 204 −10.7 −9.9
Brapa_ESTC016027 AT2G46450 ATCNGC12 (cyclic nucleotide gated channel 12) 707 70 15 15 −46.8 −4.5
Brapa_ESTC006382 AT5G45340 CYP707A3 (cytochrome P450, family 707, subfamily A, polypeptide 3) 4,649 906 962 220 −4.8 −4.1
Brapa_ESTC004877 no_hits_found --------- 315 161 100 40 −3.2 −4.0
Brapa_ESTC012086 AT4G16260 Glycosyl hydrolase family 17 protein 7,703 764 523 272 −14.7 −2.8
Broccoli Brapa_ESTC014184 AT5G49360 BXL1 (BETA-XYLOSIDASE 1); hydrolase, hydrolyzing O-glycosyl compounds 847 141 34 18 −25.1 −7.9
Brapa_ESTC002586 AT4G35770 DIN1 | SEN1 (DARK INDUCIBLE 1) 6,771 562 22 135 −303.4 −4.2
Brapa_ESTC016027 AT2G46450 CNGC12, ATCNGC12 | ATCNGC12 (cyclic nucleotide gated channel 12) 707 70 7 12 −106.0 −5.9
Brapa_ESTC021555 AT4G15530 PPDK (PYRUVATE ORTHOPHOSPHATE DIKINASE) 4,100 604 310 100 −13.2 −6.1
Brapa_ESTC007363 AT4G37010 Calcium ion binding 1,109 145 77 26 −14.4 −5.5

Genes that are differentially expressed in all experimental samples as well as both June and October samples.

Br_SEQ_ID At Locus Description Fold change
Mustard/Chiifu Turnip/Chiifu Broccoli/Chiifu
June Oct. June Oct. June Oct.
Brapa_ESTC049008 AT1G49500 Hypothetical protein 34.5 3.0 29.6 5.4 7.0 5.7
Brapa_ESTC016027 AT2G46450 CNGC12 −7.0 −6.1 −46.8 −4.5 −106.0 −5.9
Table 1 Functional categorization of DEGs by different rootstocks.
Table 2 Top 5 genes that were commonly regulated in both June and October samples.
Table 3 Genes that are differentially expressed in all experimental samples as well as both June and October samples.

Table 1

Table 2

Table 3

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