臺灣博碩士論文加值系統

豌豆蚜為研究發育、演化及生態的新興模式昆蟲物種。相較於其他現有的模式昆蟲，豌豆蚜有著異乎尋常的基因重複現象。超過 2,000 個基因家族在豌豆蚜基因體中已被確認具有廣泛的重複現象，這其中包含了生殖基因 (germline gene) 與胺基酸轉運蛋白基因 (amino acid transporter gene)，也是本論文主要研究的標的基因。我推測這兩類基因的重複現象，對於維持蚜蟲複雜的生殖週期與內共生菌間營養的交換是必要的。因此，選殖重複基因並解析其發育表現，探討從無性轉換至有性生殖階段中，生殖細胞的發育與胺基酸的傳輸成為本論文的中心議題。

我註解了八個重複的 piwi 基因及兩個 argonaute-3 (ago3) 基因，此二基因產物的保守性功能在生殖細胞中為參與 Piwi-interacting RNA (piRNA) 的形成及抑制跳躍子的活性。Appiwi2，Appiwi6 及 Apago3a 在無性世代處女蚜胚胎 (embryo of virginoparae) 中專一地表現於生殖細胞中，而序列上與它們各自最相近的重複基因 Appiwi5，Appiwi3 及 Apago3b 則非生殖細胞專一表現。從無性胎生轉換至有性卵生的過渡型蚜蟲 (transitional morphs) 中，Appiwi2 在產性蚜胚胎 (embryos of sexuparae) 與產卵蚜胚胎 (embryos of oviparae) 中保持專一表現在生殖細胞中，但是 Appiwi6 及 Apago3a 的 mRNAs 則任意分佈於胚胎之中。這暗示著：(1) 在有性與無性階段的轉換，Appiwi2 維持 piRNA 在生殖細胞中保守性功能；(2) 重複的 piwi 及 ago3 旁系同源基因獲得將 piRNAs 的功能發揮在體細胞上的新任務；以及 (3) 在產性蚜胚胎與產卵蚜胚胎中，Appiwi6 與 Apago3a 的表現差異為對光週期改變所引發的結果，且兩者隨著生殖階段的改變，可能和參與胚胎細胞 (包含了生殖細胞與體細胞) 的重新設定有關。相似的基因表現模式亦出現在重複的 nanos 基因中 - 整個生活史中，Apnanos2 似 Appiwi2 全為生殖細胞專一表現，但Apnanos1 似 Appiwi6 在產卵蚜胚胎中，則不再偏向於生殖細胞中表現。

在重複的胺基酸轉運蛋白基因中，我首先選擇研究 ApGLNT1 因其為目前所有胺基酸轉運蛋白基因中唯一有功能性上的研究 - 也就是經由嵌合在懷菌細胞膜上進行傳輸麩醯胺酸 (glutamine)。在無性胎生的胚胎中，不論 ApGLNT1 的 mRNA 或蛋白皆可在懷菌細胞上被偵測。然而，不同於 ApGLNT1 蛋白限制性地環繞於豌豆蚜成蟲的懷菌細胞膜上，ApGLNT1的表現只在胚胎懷菌細胞間的鞘細胞之細胞質中。這意味著供應胚胎必需胺基酸的來源為母體而非胚胎本身的內共生菌。除了 ApGLNT1，我亦對另外兩個尚未被分析功能的胺基酸轉運蛋白基因 – ACYPI000536 及 ACYPI008904 剖析它們在胚胎中的發育表現。出乎意料的是，此二基因的表現可在囊胚後端被偵測，而此處亦為母源內共生菌進入原腸形成期胚胎中的位置。這暗示著胺基酸轉運蛋白基因可能扮演著形成懷菌細胞前提供內共生菌侵入胚胎的位置線索。此三個重複的胺基酸轉運蛋白基因尚未在產性蚜胚胎與產卵蚜胚胎中進行表現分析。

總而言之，本論文探討了重複的生殖基因– Appiwi, Apago3 及 Apnanos在不同的繁殖型豌豆蚜中發現有差異性的基因表現。這種在生殖基因表現上的發育可塑性，意味著在不同的繁殖模式相關的特定條件下，改變生殖細胞譜系轉錄組是必須的。而發育的可塑性是否存在於體細胞基因的表現目前尚無定論。欲在豌豆蚜與其他蚜蟲中瞭解重複基因在發育中所扮演的角色，發展對於生殖基因與體細胞基因可行的功能性試驗工具無疑為現在的當務之急。

The pea aphid Acyrthosiphon pisum is an emerging insect model for developmental, evolutional, and ecological studies. In comparison with other existing model organisms, A. pisum has extraordinary gene duplication. More than 2000 gene families with extensive gene duplication have been identified in its genome. These include germline genes and amino acid transporter (AAT) genes – the targets of my study. I presume that gene duplication is required for sustaining the complicated reproductive cycle and nutritional interaction with the endosymbionts. Accordingly, cloning and developmental characterization of duplicated genes for germline development and amino acid transportation from asexual to sexual reproduction phases becomes the central issue of research.

I annotated eight copies of piwi and two of argonaute-3 (ago3), both of whose products are components of the conserved Piwi-interacting RNA (piRNA) machinery suppressing the activity of transposons in the germ cells. Expressions of Appiwi2, Appiwi6, and Apago3a in the embryos of virginoparae were “specialized” in germ cells whilst transcripts of their most closely related copies, respectively Appiwi5, Appiwi3, and Apago3b, were not germline specific. In the embryos of sexuparae and oviparae, the transitional morphs from asexual viviparity to sexual oviparity, expressions of Appiwi2 remained specific to the germ cells but Appiwi6 and Apago3a mRNAs were randomly distributed in the embryos. This suggests that: (1) Appiwi2 plays a conserved role in the piRNA pathway in germ cells throughout asexual and sexual phases; (2) duplicated piwi/ago3 paralogs obtain novel roles for exerting piRNAs functioning in the somatic cells; and (3) differential expressions of Appiwi6 and Apago3a in the embryos of sexuparae and oviparae respond to the change of photoperiods and both genes may participate in the reprogramming of embryonic cells, including germline and soma, during the change of reproduction phases. Similar expression patterns occurred to duplicated nanos genes – Apnanos2, like Appiwi2, was germline specific all over the life cycles, but expression of Apnanos1, like Appiwi6, was no longer preferentially detected in germ cells in the embryos of oviparae.

Among the duplicated AAT genes, I first selected to study ApGLNT1 for it was so far the sole AAT gene whose function—transportation of glutamine via the ApGLNT1 protein chelated to the bacteriocyte membrane—had been studied. In parthenogenetic and viviparous embryos, both of the ApGLNT1 mRNA and ApGLNT1 protein could be detected in the bacteriocytes. However, unlike restriction of ApGLNT1 to the membrane surrounding the adult bacteriocytes, expression of ApGLNT1 was only identified in the cytoplasm of the sheath cells intervening the embryonic bacteriocytes. This suggests that provision of essential amino acids to the embryos relies on the mother but rather the embryonic endosymbionts themselves. Apart from ApGLNT1, I also studied developmental expressions of ACYPI000536 and ACYPI008904, another two AAT genes whose functions have not been analyzed. Surprisingly, transcripts of both genes could be identified in the posterior region of blastula, into which the maternal endosymbionts would penetrate during gastrulation. This implies that expression of AAT genes might play a positional cue for endosymbiont invasion before the formation of bacteriocytes. Expressions of these three duplicated AAT genes in sexuparae and oviparae have not been characterized.

In summary, I studied developmental expressions of duplicated germline genes Appiwi, Apago3 and Apnanos in the pea aphid, finding differential expressions in distinct reproductive morphs. The developmental plasticity of germline gene expressions suggests that the change of transcriptome within the germline cell lineage is required for particular events associated with different types of reproduction. Whether developmental plasticity also occurs to somatic gene expressions remains an open question. Development of feasible tools for functional assays of both germline genes and somatic genes is surely an urgent call for understanding the developmental roles of all duplicated genes in A. pisum and other aphid species.

摘要 ……………………………………………………………………………. i
Abstract…………………………………………………………………………. iii
Contents ...……………………………………………………………………… vi
List of Figures.………………………………………………………………….. x
List of Tables...…………………………………………………………………. xii
List of Appendix………………………………………………………………... xiii
Chapter 1 Introduction ..………………………………………………………. 1
1. The basic concept of aphid biology………………………………………. 1
2. The pea aphid Acyrthosiphon pisum as a model organism …………….. 4
2.1 The developmental plasticity ………………………………………….. 5
2.2 The symbiosis of aphid/Buchnera……………………………………… 6
3. The comparison of asexual and sexual oogenesis and embryogenesis… 7
3.1 The morphological differences in oocytes and germaria ……………… 8
3.2 The morphological differences in sexual and asexual embryos ………. 8
3.3 Incorporation of symbiont……………………………………………… 10
4. Germ cell development…………………………………………………… 11
4.1 Germ cell development in the insect…………………………………… 11
4.2 Germ cell development in the pea aphid……………………………….. 13
5. The amino acid transporter genes and aphid symbiosis ………………. 14
6. Research purpose ………………………………………………………… 16
Chapter 2 Materials and Methods ……………………………………………. 18
1. Gene annotation of pea aphid genome ………………………………….. 18
2. Aphid lines and culture condition ……………………………………….. 18
3. Gene cloning and sequence analysis …………………………………….. 18
4. Real-time reverse transcription PCR …………………………………… 19
5. Riboprobe synthesis………………………………………………………. 21
6. Whole-mount in situ hybridization………………………………………. 21
7. Production and purification of antibody against ApNanos1 and ApNanos2………………………………………………………………… 22
8. Western blot……………………………………………………………….. 23
9. Immunostaining ………………………………………………………….. 24
10. Microscope and image analysis………………………………………….. 25
11. Phylogenetic tree construction…………………………………………… 25
12. nanos RNA secondary structure analysis……………………………….. 26
Chapter 3 Annotation of germline toolkit genes in the pea aphid genome… 27
1. Candidates of the germline toolkit genes……………………………….. 27
2. Germline toolkit genes in the pea aphid………………………………… 27
3. Germline toolkit genes in other hemipteran insects …………………… 28
Chapter 4 Duplicated germline genes and developmental plasticity in the pea aphid…………………………………………………………... 30
1. Piwi and ago3 genes……………………………………………………… 30
1.1 Isolation of piwi and ago3 homologs in the pea aphid …………………. 34
1.2 The somatic expression clades of Appiwi genes – Appiwi1/4/7 ………… 35
1.3 The germline expression clades of Appiwi genes – Appiwi2/5 and Appiwi3/6 ………………………………………………….………………. 35
1.4 RNA expression of Apago3 genes.……………………………………… 37
1.5 Germline specific expression of Appiwi2, Appiwi6 and Apago3a………. 37
2. Nanos genes……………………………………………………………….. 38
2.1 Isolation of nanos homologs in the asexual aphid ……………………… 42
2.2 Apnanos1 and Apnanos2 are germline specific genes in the pea aphid………………………………………………………………………. 44
2.3 RNA expressions of Apnanos1 and Apnanos2 in the embryos of sexuparae and oviparae …………………………………………………… 46
2.4 Posterior localized and germline specific expression of ApNanos2…….. 47
2.5 nanos orthologs of Myzus persicae show identical expression patterns to those of A. pisum. …………………………………………………………. 48
2.6 The 3’UTR structure of Apnanos homologs…………………………….. 49
Chapter 5 Developmental integration of embryogenesis and symbiosis …… 51
1. ACYPI000536 and ACYPI008904 are preferentially expressed in the endosymbiotic bacteria during embryogenesis ……………………….. 53
2. ApGLNT1 mRNA is expressed in the follicular epithelium and the bacterial sheath cells .…………………………………………...……….. 54
3. ApGLNT1 protein is localized in the maternal follicular epithelium and embryonic sheath cells ……………………………………………… 55
4. A symbiotic regulation model for the provisioning of maternal nutrition to the embryos .…………………………………………...…… 56
Chapter 6: Discussion………………………………………………………….. 57
1. Pea aphid germ cell development………………………………………... 57
2. Preservation of duplicated germline genes and developmental plasticity………………………………………...………………………… 58
2.1 Biological significance of gene duplication...…………………………. 58
2.2 Environmental cues trigger developmental plasticity under the epigenetic regulation………………………………………...…………. 60
2.3 Germline gene duplication events may happen with evolving the cyclic parthenogenesis at the same time………………………………………. 61
3. The potential function of germline duplicated genes in the pea aphid.. 62
3.1 Diversification of developmental expression of Piwis in the germline and soma……………………………………………………………….. 62
3.2 Diversification of expression profiles is correlated with the reproductive mode……………………………………………………... 64
3.3 Apnanos2 retains the function in germline development ……………… 65
3.4 The phylogenic relationship between insect nanos orthologs…………. 66
3.5 Duplicated nanos are not involved in segmental regulation…………… 67
3.6 Differentially expressions of Apnanos are related to the developmental plasticity………………………………………………………………... 68
3.7 nanos1 and nanos2 are germline-specific but may possess different functions………………………………………………………………... 69
3.8 cis-translational control in the pea aphid ……………………………… 69
3.9 Differential expressed germline genes are involved in the meiosis between aphid morphs. ……………………………………………….. 70
4. Amino acid transporter gene duplication and symbiosis………………. 72
4.1 Gene duplication to facilitate symbiosis maintenance…………………. 72
4.2 Maternal and embryonic bacteriomes are not equivalent……………… 73
4.3 Nutrients provisioning to the asexual pea aphid embryo are from maternal symbiosis and possible embryonic symbiosis…………...…... 74
4.4 The translocation of ApGLNT1 protein from bacterial sheath cells to bacteriocytes …………………………………………………………... 76
4.5 Amino acid transporter as a sensor or signal molecule………………… 77
4.6 Symbiosis and asexual aphid reproduction…………………………….. 78
5. Tools for post-genomic functional assay……………………………….... 79
6. Potential approaches to test the results of studied duplicated genes….. 81
References………………………………………………………………………. 84
Figures.………………………………………………………………………….. 121
Tables…..……………………………………………………………………….. 172
Appendix………………………………………………………………………... 184

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