RESEARCH ARTICLE Open Access Genome wide identification, evolution and expression analysis of the aspartic protease gene family during rapid growth of moso bamboo (Phyllostachys edulis) shoots Xiaqin[.]
Wang et al BMC Genomics (2021) 22:45 https://doi.org/10.1186/s12864-020-07290-7 RESEARCH ARTICLE Open Access Genome-wide identification, evolution and expression analysis of the aspartic protease gene family during rapid growth of moso bamboo (Phyllostachys edulis) shoots Xiaqin Wang1,2,3, Xinyang Yan1,2, Shubin Li1, Yun Jing1, Lianfeng Gu1, Shuangquan Zou1,2, Jin Zhang3* and Bobin Liu1,2* Abstract Background: Aspartic proteases (APs) are a class of aspartic peptidases belonging to nine proteolytic enzyme families whose members are widely distributed in biological organisms APs play essential functions during plant development and environmental adaptation However, there are few reports about APs in fast-growing moso bamboo Result: In this study, we identified a total of 129 AP proteins (PhAPs) encoded by the moso bamboo genome Phylogenetic and gene structure analyses showed that these 129 PhAPs could be divided into three categories (categories A, B and C) The PhAP gene family in moso bamboo may have undergone gene expansion, especially the members of categories A and B, although homologs of some members in category C have been lost The chromosomal location of PhAPs suggested that segmental and tandem duplication events were critical for PhAP gene expansion Promoter analysis revealed that PhAPs in moso bamboo may be involved in plant development and responses to environmental stress Furthermore, PhAPs showed tissue-specific expression patterns and may play important roles in rapid growth, including programmed cell death, cell division and elongation, by integrating environmental signals such as light and gibberellin signals Conclusion: Comprehensive analysis of the AP gene family in moso bamboo suggests that PhAPs have experienced gene expansion that is distinct from that in rice and may play an important role in moso bamboo organ development and rapid growth Our results provide a direction and lay a foundation for further analysis of plant AP genes to clarify their function during rapid growth Keywords: Aspartic protease, Moso bamboo, Programmed cell death, Rapid growth * Correspondence: zhangj@zafu.edu.cn; liubobin@fafu.edu.cn State Key Laboratory of Subtropical Silviculture, School of Forestry and Biotechnology, Zhejiang A&F University, Zhejiang 311300, Hangzhou, China College of Forestry, Fujian Agriculture and Forestry University, Fuzhou 350002, China Full list of author information is available at the end of the article © The Author(s) 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data Wang et al BMC Genomics (2021) 22:45 Background Aspartic proteinases (APs; Enzyme Commission 3.4.23) are proteolytic enzymes and play important roles in protein maturation and degradation [1, 2] The majority of APs have two conserved motifs with catalytic activity: an Asp-Thr-Gly (DTG) motif and an Asp-Ser-Gly (DSG) motif [3, 4] APs are widely distributed among microbes, mammals and plants [3, 5] and are divided into 16 subfamilies based on their tertiary structure and evolutionary relationships [4, 6] APs are involved in many important biological processes that are involved in development, nutrition, pathogenesis, disease and so on and have potential for commercial application [7, 8] Most plant APs are grouped into the A1 family and exhibit the two basic features of A1 family members: one features is that they are active under acidic conditions, and the other is that their catalytic activity can be specifically inhibited by pepstatin A [1, 9] Since the 1980s, plant APs have been purified via pepstatin Aagarose columns and detected in various plant species [3, 4, 10] Plant APs can be classified into three categories: typical APs, nucellin-like APs and atypical APs [1, 9] Typical APs contain a plant-specific insert (PSI) similar to that of saposin-like proteins, but it is removed during protein maturation [1, 2] Nucellin-like APs are similar to nucellins in barley ovules [11] The characteristics of atypical APs are intermediate between those of typical and nucellin-like APs [9, 12] Pepstatin A activity has been detected in immature, mature, and germinated seeds in wheat, and the expression pattern showed a role of APs in regulating protein degradation [13, 14] Plant APs are also considered to be responsible for protein processing and degradation, such as plant senescence, programmed cell death (PCD), reproduction, and stress responses [2, 15–20], which are critical for plant development With the development of DNA sequencing technology, members of plant AP gene families have been identified in Arabidopsis [9], rice [12], grape [21], and poplar [22], revealing gene expansion and functional diversity [12, 22] The function of plant APs has been determined primarily in seeds, including dormant seeds and different parts of seeds [10, 14, 23, 24] It was proposed that, during seed development, plant APs are involved in seed storage protein processing on the basis of the 2S albumin process in vitro and colocalization with proteins in the plant body [25] During seed germination, plant APs are considered to be involved in seed storage protein degradation [26–28] Recently, Arabidopsis ASPARTIC PROTEASE IN GUARD CELL (ASPG1) was reported to promote seed germination by accelerating the breakdown of seed storage proteins [28] In addition to their involvement in seed development and germination, APs participate in the degradation of insect proteins, allowing Page of 20 carnivorous plants to obtain nitrogen from those sources [15, 29] Plant APs also play roles in the response to biotic and abiotic stresses ASPG1 is abscisic acid (ABA) inducible, and Arabidopsis plants overexpressing this gene had in increased ability to resist drought stress because of the participation of the transgene in ABA-dependent responsiveness [17] Constitutive Disease Resistance (CDR1), an atypical plant aspartic proteinase, exhibits the ability to induce systemic defense responses against bacterial and fungal pathogens in rice and Arabidopsis [20, 30, 31] Ectopic expression of VqAP13, a grape aspartic protease gene, can afford powdery mildew resistance but reduces Botrytis cinerea resistance by regulating the salicylic acid and MeJA signaling pathways [19] Plant APs also play roles in plant development, such as reproduction and lateral root formation OsAP65 has been proposed to be involved in biosynthesis of compounds that are essential to pollen germination and pollen tube growth in rice [32] Two novel AtAPs in Arabidopsis (A36 and A39) have been speculated to participate in gametogenesis and pollen guidance [18] Recently, an atypical aspartic protease, Atypical Aspartic Protease in Roots (ASPR1), was determined to suppress primary root growth and lateral root development [33] Altogether, plant APs are important proteins that are involved in various aspects of plant development and responses to environmental changes Some plant APs also play an important role in regulating PCD In barley, a gene encoding an aspartic protease-like protein (‘nucellin’) was highly expressed after pollination, which was synchronized to nuclear cell degeneration characteristic of PCD [11] Phytepsin, a vacuolar aspartic proteinase that is a plant homolog of cathepsin D and mediates PCD in barley, is highly expressed during the active autolysis of the root cap and in tracheary elements and sieve cells [34] In rice, the transcripts of OsAP25 and OsAP37 in anthers are activated by ETERNAL TAPETUM (EAT1) to regulate PCD in tapetal cells [35] In Arabidopsis, PROMOTION OF CELL SURVIVAL (PCS1) encodes an aspartic protease, and compared with wild type, loss-of-function mutants experience gametophyte degeneration and cell death of developing embryos [36] AP proteins have also been identified in the plant cell wall, and cis-elements related to secondary cell wall (SCW) thickening and PCD, such as SNBE, TERE, and SMRE, were discovered upstream of partial AP genes from poplar, strongly suggesting that APs play important roles in SCW and PCD [37–41] To date, there are many reports on plant AP function in model plant species such as Arabidopsis and rice However, the function of APs in rapid-growing plant species such as bamboo is still unclear Bamboo is a member of the Gramineae family, is widely distributed worldwide and is a rapid-growing plant species Bamboo forests can provide young Wang et al BMC Genomics (2021) 22:45 bamboo shoots for food, fibrous raw material, building materials, raw materials for furniture and crafts and so on within a short time [42] In addition to its economic benefits, bamboo also has important ecological functions, such as the ability to restore degraded landscapes and combat global climate change [42, 43] The moso bamboo (Phyllostachys edulis) planting area is approximately 3.27 million and constitutes most of the bamboo forest region in China [43] Rapid growth of moso bamboo occurs after the young bamboo shoots are covered with a shell and emerge from the ground PCD was revealed to occur in pith cavity formation during rapid bamboo growth [44] During the bamboo rapid-growth stage, cell division gradually decreases, while cell elongation and secondary cell wall thickening also occur [45, 46] Therefore, PCD and SCW formation are important biological events during rapid growth of moso bamboo Members of the NAC, MYB and LAC gene families have been identified as being associated with SCW in moso bamboo [47, 48] The MYB gene family has specifically been reported to be involved in environmental responses [49] In addition to rapid growth, the flowering pathway [50, 51] and sucrose synthase [52] have also been widely studied in bamboo Recently, a chromosome-level de novo genome assembly of moso bamboo was provided, which, compared with the previous version, was obviously improved in terms of the assembly data and quality of the whole-genome sequencing assembly [43, 53] The release of new bamboo genomic data allows us to perform genome-wide gene functional analyses in moso bamboo Here, we identified a total of 129 PhAP proteins that contain a conserved Asp domain from the moso bamboo genome Phylogenetic analysis revealed that PhAP genes might have experienced gene expansion via segmental and tandem duplication Gene structure and motifs indicated that the motifs of PhAPs were conserved, although the gene structure has changed throughout evolutionary history Expression pattern analysis showed that PhAPs exhibited tissue-specific expression patterns, and several sets of PhAPs may play important roles during moso bamboo rapid growth Our study provides a strong foundation for further research on the potential function of these proteins in bamboo development and an improved understanding of the AP gene family in fast-growing nontimber forest species Results Genome-wide identification of AP genes from the moso bamboo genome After two rounds of moso bamboo genome searching via HMMER v3 (the details of which are in the materials and methods), a total of 129 Asp family proteins with a conserved Asp domain were analyzed via the NCBICDD and Pfam database (Fig and Table S1) Among Page of 20 these Asp proteins, 102 had two catalytic sequence motifs, Asp-Thr-Gly (DTG) and Asp-Ser-Gly (DSG), which are typical features of aspartic proteases; however, 18 proteins contained one catalytic motif, and nine proteins had no motif (Fig and Table S1) Moso bamboo Asp genes were named based on their relationships with homologous genes in rice and are listed in Table S1 Other information on the members of the Asp gene family, including their chromosomal localization, CDS, amino acid residue sequence, corresponding protein length, corresponding protein molecular weight, and corresponding protein isoelectric point, is also listed in Table S1 Phylogenetic relationships among the 129 moso bamboo Asp proteins were determined using an IQ-TREE procedure [54] The 129 moso bamboo Asp proteins fell into three distinct categories (pink, blue and purple clades) and were termed categories A, B and C, respectively (Fig 1) From the predicted protein domain, we found that all PhAPs contained one Asp domain of variable length (Fig 1) There were 16 moso bamboo category A PhAP members, eight of which contained signal peptides, and the Asp domain consisted of the Taxi_N and PSI domains (including SapB_1 and SapB_2) with two catalytic motifs (Fig and Table S1) However, there were no signal peptides or PSI domains and/or a lack or partial lack of catalytic motifs in the other eight category A PhAPs (Fig and Table S1) Categories B and C had 26 and 87 members, respectively, that contained the full-length Asp domain consisting of Taxi_N and Taxi_ C, except for PhAP7.4, PhAP31.3, PhAP7.2, PhAP87.1, PhAP4.1, PhAP50.3, PhAP27.2 and PhAP40.2 (Fig 1) Less than half of the category B PhAPs are nucellin-like APs containing catalytic sites (Fig and Table S1), which is similar to that which occurs rice [12] Category C, composed of atypical aspartic proteases, was the largest category (Fig 1) Most category B and C members contained a signal peptide, and it was notable that there were signal peptides and transmembrane domains located in the N- and C-termini, respectively, of nine category B AP proteins (Fig 1) Phylogenetic analysis of APs from moso bamboo and rice To investigate the evolutionary relationship of the PhAP family, a phylogenetic tree was constructed using 129 PhAP and 92 OsAP full-length amino acid residue sequences (Table S1 and Table S2) Both PhAPs and OsAPs were classed into three categories, as previously reported in Arabidopsis [9], rice [12], grape [21] and poplar [22] Category A contained 16 PhAPs together with seven OsAPs; these proteins could be classified into seven subclades based on their relationships with their rice homologous proteins (Fig 2) There was at least one PhAP homolog in each subclade but no homolog of OsAP6 (Fig 2) The moso bamboo genome encoded eight PhAP88 genes and only one homolog in rice, which meant that AP88 underwent gene expansion in moso bamboo (Fig 2) 25 PhAPs and 15 OsAPs Wang et al BMC Genomics (2021) 22:45 Page of 20 prot ein_dom ain 100 100 99 100 Asp SapB_1 SapB_2 TAXi_C TAXi_N signal pept ide t ransm em brane dom ain PPR repeat DYW_deam inase Met hylt ransf_29 ATP-synt _G Pect inest erase RRM_8 DXP_synt hase_n 99 92 100 100 100 94 60 81 97 100 100 78 100 100 100 99 63 85 90 100 100 98 92 100 95 71 100 100 100 100 53 100 65 67 64 74 74 65 83 37 68 100 100 100 100 100 100 39 26 100 100 94 91 93 57 49 58 100 99 100100 99 54 100 84 56 100 74 54 60 69 100 57 75 100 49 100 100 99 62 99 44 100 100 83 100 100 100 100 100 97 99 100 97 57 100 97 81 43 94 98 100 100 100 100 84 98 100 100 91 100 100 98 98 92 91 99 99 96 100 100 100 Fig (See legend on next page.) PhAP22.2 PhAP22.1 PhAP53.1 PhAP53.2 PhAP91.1 PhAP70.1 PhAP70.2 PhAP68/76.1 PhAP8/21.1 PhAP8/21.2 PhAP8/21.3 PhAP8/21.4 PhAP48.1 PhAP49.1 PhAP57.1 PhAP57.7 PhAP57.2 PhAP57.6 PhAP57.3 PhAP57.4 PhAP57.5 PhAP20.1 PhAP20.2 PhAP58.2 PhAP58.1 PhAP56.3 PhAP56.1 PhAP56.2 PhAP73.1 PhAP58/73.1 PhAP66.2 PhAP66.1 PhAP17.1 PhAP25.2 PhAP25.1 PhAP14.2 PhAP14.1 PhAP7.2 PhAP7.1 PhAP7.3 PhAP45.2 PhAP45.1 PhAP87.1 PhAP4.2 PhAP4.1 PhAP39.2 PhAP39.1 PhAP16.1 PhAP16.2 PhAP16.3 PhAP71.2 PhAP71.1 PhAP69.1 PhAP87.2 PhAP93.1 PhAP93.2 PhAP93.3 PhAP93.4 PhAP93.5 PhAP93.6 PhAP64.1 PhAP50.3 PhAP50.2 PhAP50.1 PhAP32.1 PhAP27.1 PhAP27.2 PhAP28.1 PhAP32.2 PhAP72.1 PhAP72.2 PhAP72.3 PhAP37.1 PhAP36.1 PhAP36.2 PhAP61.1 PhAP13.1 PhAP5.1 PhAP5.2 PhAP43.2 PhAP43.1 PhAP12.3 PhAP12.2 PhAP12.1 PhAP18.1 PhAP40.2 PhAP40.1 PhAP65.1 PhAP65.2 PhAP15.2 PhAP15.1 PhAP19.2 PhAP19.1 PhAP35.1 PhAP24.1 PhAP74.2 PhAP74.1 PhAP31.2 PhAP31.1 PhAP59.3 PhAP59.2 PhAP59.1 PhAP7.4 PhAP31.3 PhAP23.2 PhAP23.1 PhAP52.2 PhAP52.1 PhAsp3.2 PhAsp3.1 PhAsp1.1 PhAsp2.2 PhAsp2.1 PhAP44/90.1 PhAP44/90.2 PhAP44/90.3 PhAP10.1 PhAP9.2 PhAP9.1 PhAP41.2 PhAP41.1 PhAP88.7 PhAP88.8 PhAP88.6 PhAP88.2 PhAP88.1 PhAP88.5 PhAP88.4 PhAP88.3 C B A Wang et al BMC Genomics (2021) 22:45 Page of 20 (See figure on previous page.) Fig Phylogenetic relationships and protein domain diagram of moso bamboo aspartic proteinases The left part shows the phylogenetic relationships of 129 APs from moso bamboo Categories A, B And C are shaded in pink, blue and purple, respectively The blue stars, red triangles and green circles represent APs containing 2, and catalytic sequences, respectively Bootstrap are shown close to the branch nodes The right part shows the protein domain, and the caption is shown in the upper left corner There were no homologous genes of OsAP77–87 in moso bamboo, indicating that the homologs in bamboo were lost during evolutionary history (Fig 2) Altogether, these results showed that the PhAP gene family in moso bamboo underwent specific evolutionary events after the divergence of bamboo and rice 66 84 83 85 100 97 71 100 AP P9 0 h P h A APP1 P s A P4 O h A 4/ P s AP / O s AP 4 / 10 O h AP 4 Ph P P h A P4 P sA P4 O h A P4 P h A P8 96 75 92 P sA 8 O h AP 8 9 P h AP 8 P h AP P h AP8 51 0 P AP8 Ph AP8 9 Ph AP8 Ph AP8 8 95 98 Ph AP6 Os A 99 10 84 93 78 64 OsAP31 55 90 77 100 PhAP3 1.2 98 100 PhAP31 OsAP74 99 95 Ph AP74 10 Ph A 82 OsA P7 1 07 58 Ph P5 100 Ph AAPP5 9 Ph 100 Os AP5 71 66 Ph AAP2 P 76 P 9 18 O h AP3 00 O sAP 71 00 OssAP33 P A O h A P3 10 PhsAPP3 A P 10 O h A P1 Ph sAPP1 99 10 100 P A O h P 15 100 P s AP 00 P h AA P 100 2 P5 sA P O A P Ph h A Aspp 33 P s As p O h As p P h As p P 99 Osh Assp 21 P h A sp P sA sp 10 O A 0100 PhsAP 10 O h AP 00 P P 10 PhsAAP47 99 O sAP 10 O P6 OshAAP6 / 99 P AP7 78 Os 84 Ph AAPP7 86 00 Ph AP8 00 s 21 O Os A P 1 100 Ph AP88//221 Ph AP Ph AP8/ 21 PhAP8/ 21 OsAP48 O P O s P h s AP Ph h AAP5AP8 2 P O AP 6 O sA Ph AP Os sAPP5 10 P AP 5 Phh AP / 99 AP 10 O 99 50 Ph sA AP P5 10 73 49 sAP PhO 10 Ph AAP2 P2 0 Os A 77 Ph P 100 Ph AP5 72 100 Ph AAPP5 45 48 Ph AP 00 Ph AP 38 Ph AP Ph AP5577 99 100 94 00 OsAP5.1 100 Ph AP48 97 OsAP47 43 PhAP49.1 98 95 OsAP49 100 100 86 74 10 10 52 10 O Ph O sA APsA P6 O P s P6 Ph h A AP A P5 10 OsOsAP5 10 O A Ph sA P3P51 10 P AP P Phh AP11 6 10 AP 10 00 O Ph sAP6 69 85 A Os P1 1 A 0 PhOsAPP1 0 00 Ph AAP4 31 1 P O Ph sAP4 0 Ph AAP1 13 100 100 83 Ph APP1 2 OsA1P21.3 10 0 95 Ph AP7 42 Ph AP4 Ph AP45 10 OsAP45 10 PhAP7.3 70 100 99 PhAP7.1 100 100 95 PhAP7.2 69 OsAP7 10 0 Ph AP14 10 84 Ph AP14 OsAP4 1 0 0 Ph AP Ph AsPA4P4 O 99 99 P A Ph P3 29 Ph AsAP3 1 01 0 0 O P2 Ph AAP2 52 00 100 PhOsAP7 1 0 17 10 10 P AP Ph A Os P6 66 00 98 A 10 Phh AP6AP6 1 s P O 91 100 AP P 10 Ph OssAAPP5 00 O sA 10 O AP 5 P P Ph h A sA 2 2 P O AP P Ph h A P 68 C PhAP72.2 100 90 PhAP72 100 90 OsAP72 93 Ph AP320.2 75 Ph AP5 77 Ph AP 100 Ph AP5 97 OsA3P2 Ph AP 1 0 9 Ph APP2 100 Ph AsAP2.71 100 O P2 8 00 Ph A AP2 s O AP 00 00 99 Os P2 A 76 OssAP31 1 O 99 AP 1 96 Ph AP7 P7 76 Ph OsA 9 10 AP AP 10 Ph Os sAPP7 10 O A 3 Os P1AP11 1 A Ph OsAP6AP6 s Ph O PhAP72.3 OsAP36 Ph AP36 Ph AP36 OsAP6 100 Os A P Ph AP66 100 84 Os A P 07 01 0 93 Ph Ph AP9 95 Ph AAP9 P P 95 00 P h AP9 P h AP PhhAAP9933 98 83 83 P P 99 10 O h AP 00 O sA OssAPP8 O A O sA P8 10 98 O sA P OssA P88 10 P O O s AP O s A O sAAPP8 O sA P sA P 7 P9 were classified into category B, which could be further divided into 13 subclades (Fig 2) Each subclade contained at least one PhAP homolog in moso bamboo (Fig 2) Category C contained 87 PhAPs and 70 OsAPs There was at least one PhAP homolog, and PhAP57 and PhAP93 exhibited evidence of gene expansion in moso bamboo (Fig 2) Oh P s A P6 Ph h A APP6 5 AP P2 23 .1 B Fig Phylogenetic tree of moso bamboo and rice aspartic proteinases Categories A, B and C are shaded pink, blue and purple, respectively The blue stars and green circles represent moso bamboo APs and rice APs, respectively The bootstrap percentages are shown close to the branch nodes (2021) 22:45 Page of 20 Chromosomal location and gene duplication events of PhAPs Ch PhAs p2.2 PhA P74 25 PhA PhA P71 P70 50 Ch r 50 25 Ch r5 r21 Ch Chr 50 P20 Chr2 25 PhAP Ch r3 Ch 75 PPhA Ph P P hAAP 20 10 PPhhAAPP88/ /21.1 0 hAPP222.221.1.2 243.2 P 25 PhhA Ph APP6 AP 65 6.2 61 1 50 25 Chr2 r2 P 25 P h P h A PhhAAPP228 11 APP2 .1 00 127.12 50 Chr1 r23 25 AP PhAP40.1 PhAP39.1 PhAP7.4 50 PhAP88.2 PhAP36.2 25 P353.1 PhA P9 3.6 PhA PhAAPP31.1 Ph 75 P88 PhA P31 50 PhA 36 AP 7.1 PhhAP3 P 39 AP 40 PhhAP P Ph PhA Chr24 25 the maximum number of PhAP genes; 13 PhAP genes were on chromosome 8; 12 PhAPs were on chromosome 14; and chromosomes 2, 5, and 11 had only one PhAP gene (Fig 3) There was no PhAP gene located on chromosome 1, 19, or 22 (Fig 4) Segmental and tandem duplications are considered to be the main reasons leading to gene family expansion in plants As shown in Fig 3, some PhAP genes (PhAP8/21.1 and PhAP8/ 21.2; PhAP57.2 and PhAP57.3; and PhAP57.4, We mapped the PhAPs onto chromosomes to examine the PhAP distribution on the moso bamboo chromosomes Among the 129 PhAP genes, 124 were located on 21 out of 24 moso bamboo chromosomes, while the other five PhAPs were located on scaffolds (Fig 3) Figure shows that the chromosomal distribution of the PhAPs was nonrandom but was scattered and uneven Fourteen PhAPs located on chromosome contained 25 Wang et al BMC Genomics 25 PhAP43.2 50 PhAP44/90.1 Chr18 PhAP70.2 PhAP71.1 PhAP72.2 PhAP74.1 25 Chr7 25 Chr19 19.1 87 AP 88.8.1 h P P 50 PhAAP448.1.2 h P PPhAAP3520.22 h P hAPP52 P A 53 25 PhhAPP57 12 P hA P57 P hA 57 P 50 PPhAAP578.2 PhhAP5 9.3 P hAP5 9.2 75 P PhAP Chr8 PhAP41.1 100 Chr Chr1 75 18.1 PhAP 19.2 50 PhAP 21 25 P8/ /21.4 PhhAAP8P223.1.1 P PhAAP2 Ph 11 AP PhhAPP5.2 10 P hA P 8 75 AP Ph .1 AP P9 0.1 h P hA P1 P hA P AP Ph r Ch r12 Ch Ph As p3 Chr1 Chr14 PhA PhA P4.21 PhAPP17.1 00 PhAP1 6.1 PhAP145.2 75 PhAP13 1 PhAP12 PhAP12 50 PhAP9 PhAP7.2 25 PhAP88 PhAP31 25 r15 AP 10 P 44/ PhhAP 90.3 Ph AP 25 Ph AP 16 75 AP 88 32 5 Ch 11 25 p3 As 3.4 Ph P9 3.32 A PhhAPP933.1 25 PPhAAP9 Ph 91 50 hAPsp2 .1 PPhAAsp1 Ph 25 P45 PhA 72.3 50 PhAPP69.1 PhA 75 8/76.1 PhAP6 100 PhAP72.1 125 Ph 25 50 Ph PPhhAAPP43 Ph AP444/ P 25 PhhAAPP6 5.2 0.2 AP 656.1 50 r1 16 Ch r Ch P Ph hA APP1 50 6.2 PhAP7.2 PhAP50.1 PhAP52.1 PhAP53 25 Ph AP58/7 PhAP 56.3 3.1 PhAP56 50 PhAP56 Ph Ph AP57.5 PhAAPP58.1 75 P hAP 1.2 PhAP5194.2 Fig Chromosomal location and tandem duplicated genes among 124 PhAP genes A total of 124 out of 129 PhAPs were mapped onto the chromosomes on the basis of their physical location Chromosome numbers (Chr1- Chr24) are at the bottom of each chromosome The gray lines indicate duplicated blocks, while the red lines indicate duplicated PhAP gene pairs The genes listed in red font are segmentally duplicated, while tandemly duplicated genes are shaded in green Wang et al BMC Genomics (2021) 22:45 Page of 20 PhAP22.2 PhAP22.1 PhAP53.1 PhAP53.2 PhAP91.1 PhAP70.1 PhAP70.2 PhAP68/76.1 PhAP8/21.1 PhAP8/21.2 PhAP8/21.3 PhAP8/21.4 PhAP48.1 PhAP49.1 PhAP57.1 PhAP57.7 PhAP57.2 PhAP57.6 PhAP57.3 PhAP57.4 PhAP57.5 PhAP20.1 PhAP20.2 PhAP58.2 PhAP58.1 PhAP56.3 PhAP56.1 PhAP56.2 PhAP73.1 PhAP58/73.1 PhAP66.2 PhAP66.1 PhAP17.1 PhAP25.2 PhAP25.1 PhAP14.2 PhAP14.1 PhAP7.2 PhAP7.1 PhAP7.3 PhAP45.2 PhAP45.1 PhAP87.1 PhAP4.2 PhAP4.1 PhAP39.2 PhAP39.1 PhAP16.1 PhAP16.2 PhAP16.3 PhAP71.2 PhAP71.1 PhAP69.1 PhAP87.2 PhAP93.1 PhAP93.2 PhAP93.3 PhAP93.4 PhAP93.5 PhAP93.6 PhAP50.3 PhAP64.1 PhAP50.2 PhAP50.1 PhAP32.1 PhAP27.1 PhAP27.2 PhAP28.1 PhAP32.2 PhAP72.1 PhAP72.2 PhAP72.3 PhAP37.1 PhAP36.1 PhAP36.2 PhAP61.1 PhAP13.1 PhAP5.1 PhAP5.2 PhAP43.2 PhAP43.1 PhAP12.3 PhAP12.2 PhAP12.1 PhAP18.1 PhAP40.2 PhAP40.1 PhAP65.1 PhAP65.2 PhAP15.2 PhAP15.1 PhAP19.2 PhAP19.1 PhAP35.1 PhAP24.1 PhAP74.2 PhAP74.1 PhAP31.2 PhAP31.1 PhAP59.3 PhAP59.2 PhAP59.1 PhAP7.4 PhAP31.3 PhAP23.2 PhAP23.1 PhAP52.2 PhAP52.1 PhAsp3.2 PhAsp3.1 PhAsp1.1 PhAsp2.2 PhAsp2.1 PhAP41.1 PhAP41.2 PhAP9.1 PhAP9.2 PhAP10.1 PhAP44/90.3 PhAP44/90.2 PhAP44/90.1 PhAP88.7 PhAP88.8 PhAP88.6 PhAP88.2 PhAP88.1 PhAP88.5 PhAP88.4 PhAP88.3 5' Fig (See legend on next page.) 3' 5' 100 200 300 400 500 600 700 800 900 4000 8000 Motif Motif Motif Motif Motif Motif Motif Motif 10 Motif Motif UTR CDS 3' 12000 16000 ... 43] The moso bamboo (Phyllostachys edulis) planting area is approximately 3.27 million and constitutes most of the bamboo forest region in China [43] Rapid growth of moso bamboo occurs after the. .. of these proteins in bamboo development and an improved understanding of the AP gene family in fast-growing nontimber forest species Results Genome- wide identification of AP genes from the moso. .. in the N- and C-termini, respectively, of nine category B AP proteins (Fig 1) Phylogenetic analysis of APs from moso bamboo and rice To investigate the evolutionary relationship of the PhAP family,