Abstract
Phytohormones play an important role in the pollination and fertilization of crops, but the regulatory mechanisms of oil palm pollination and fertilization are unclear. The purpose of this study is to explore the hormonal changes of oil palm pistils during flowering. We used RNA sequencing to evaluate differentially expressed genes (DEGs) in oil palm pistils at the pollination and non-pollination stages. In this study, we found that the hormone contents of oil palm pistil changed drastically after pollination. The transcriptome of the oil palm pistil without pollination and at 2 h, 4 h, 12 h, 24 h, and 48 h after pollination was comprehensively analyzed, and a large number of differential genes and metabolic pathways were explored. Based on the transcriptome data, it could be recognized that the changes of indoleacetic acid (IAA), zeatin riboside (ZR), and abscisic acid (ABA) during pollination were consistent with the changes in the corresponding gene transcripts. Differentially expressed genes during pollination and fertilization of oil palm were mainly related to energy metabolism and hormone signal transduction. It provides new insights to elucidate the interaction and regulation mechanisms of plant hormones before and after oil palm pollination, providing a theoretical basis and reference for the research on sexual reproduction of oil palm.
Similar content being viewed by others
References
Adam H, Jouannic S, Morcillo F, Richaud F, Duval Y, Tregear JW (2006) MADS box genes in oil palm (Elaeis guineensis): Patterns in the evolution of the SQUAMOSA, DEFICIENS, GLOBOSA, AGAMOUS, and SEPALLATA subfamilies. J Mol Evol 62:15–31. https://doi.org/10.1007/s00239-005-0333-7
Casanova-Sáez R, Voß U (2019) Auxin metabolism controls developmental decisions in land plants. Trends Plant Sci 24:741–754. https://doi.org/10.1016/j.tplants.2019.05.006
Chai J (2008) Studying progress of the biosynthesis and signal pathway of cytokinin. J Anhui Agricult Sci 36:3985–3989. https://doi.org/10.3969/j.issn.0517-6611.2008.10.025
Chen D, Zhao J (2008) Free IAA in stigmas and styles during pollen germination and pollen tube growth of Nicotiana tabacum. Physiol Plant 134:202–215. https://doi.org/10.1111/j.1399-3054.2008.01125.x
Chen JH, Xia XL, Yin WL (2010) PP2C-type protein phosphatases and their functions in stress signaling. J Beijing Forest Uni 32:168–171
Damayant S, Andry S, Khairurrijal KRE (2014) Isolation of β-carotene from palm (Elaeis guineensis Jacq.) oil using transesterification-adsorption-desorption method and its characterization. J Appl Sci 14:2615–2621. https://doi.org/10.3923/jas.2014.2615.2621
Daza E, Ayala-Díaz I, Ruiz-Romero R, Romero HM (2021) Effect of the application of plant hormones on the formation of parthenocarpic fruits and oil production in oil palm interspecific hybrids (Elaeis oleifera Cortes x Elaeis guineensis Jacq.). Plant Prod Sci 24:354–362
Fujita Y, Yoshida T, Shinozaki KY (2013) Pivotal role of the AREB/ABF-SnRK2 pathway in ABRE-mediated transcription in response to osmotic stress in plants. Physiol Plant 147:15–27. https://doi.org/10.1111/j.1399-3054.2012.01635.x
Gao Z, Daneva A, Salanenka Y et al (2018) KIRA1 and ORESARA1 terminate flower receptivity by promoting cell death in the stigma of Arabidopsis. Nat Plant 4:365–375. https://doi.org/10.1038/s41477-018-0160-7
Guo Y, Cui K, Qin L, Zhang XB, Tong JH, Liu ZS, Xia ST (2019) Dynamic change of phytohormones in seeds of yellow-seeded canola progeny from hybridization between Brassica Juncea and Brassica Napus and its effects on fatty acid composition and oil content. Acta Laser Biol Sinica 28:548–555. https://doi.org/10.3969/j.issn.1007-7146.2019.06.011
He D, Xie MJ, Lv BY, Wang Z, Liu YP, He SL (2017) Analysis of pollination affinity performance and its physiological mechanism in Paeonia suffruticosa and Paeonia lactiflora. J Northwest A&F Univ (Natural Science Edition) 45:129–136. https://doi.org/10.13207/j.cnki.jnwafu.2017.10.016
Heyl A, Riefler M, Romanov GA, Schmülling T (2012) Properties, functions and evolution of cytokinin receptors. Eur J Cell Biol 91:246–256. https://doi.org/10.1016/j.ejcb.2011.02.009
Hisami Y, Tomomi S, Kazunori T, Kentaro T, Kuniko I, Kumiko M, Takafumi Y, Takeshi M (2001) The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol 42:1017–1023. https://doi.org/10.1093/pcp/pce127
Honma T, Goto K (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409:525–529. https://doi.org/10.1038/35054083
Hrabak EM, Chan CWM, Gribskov M, Harper JF, Choi JH, Halford N, Kudla J, Luan S, Nimmo HG, Sussman MR, Thomas M, Walker-Simmons K, Zhu JK, Harmon AC (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132:666–680. https://doi.org/10.1104/PP.102.011999
Huang ZJ (2019) Molecular mechanism of pollen tube growth and double fertilization in angiosperm. Biol Teach 44:5–8
Hutchison CE, Li J, Argueso C, Gonzalez M, Lee E, Lewis MW, Maxwell BB, Perdue TD, Schaller GE, Alonso JM, Ecker JR, Kieber JJ (2006) The Arabidopsis histidine phosphotransfer proteins are redundant positive regulators of cytokinin signaling. Plant Cell 18:3073–3087. https://doi.org/10.1105/TPC.106.045674
Hwang I, Sheen J (2001) Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413:383–389. https://doi.org/10.1038/35096500
Jiang Y (2020) Research on the mechanism of SIPP2C in regulating tomato senescence. Shenyang Agricultural University. https://doi.org/10.27327/d.cnki.gshnu.2020.000023
Kessler SA, Shimosato-Asano H, Keinath NF, Wuest SE, Ingram G, Panstruga R, Grossniklaus U (2010) Conserved molecular components for pollen tube reception and fungal invasion. Science 330:968–971. https://doi.org/10.1126/science.1195211
Kobayashi Y, Yamamoto S, Minami H, Kagaya Y, Hattori T (2004) Differential activation of the rice sucrose nonfermenting1-related protein kinase2 family by hyperosmotic stress and abscisic acid. Plant Cell 16:1163–1177. https://doi.org/10.1105/TPC.019943
Kowalska M, Galuszka P, Frébortová J, Šebela M, Béres T, Hluska T, Šmehilová M, Bilyeu KD, Frébort I (2010) Vacuolar and cytosolic cytokinin dehydrogenases of Arabidopsis thaliana : Heterologous expression, purification and properties. Phytochem 71:1970–1978. https://doi.org/10.1016/j.phytochem.2010.08.013
Kurepa J, Li Y, Smalle JA (2014) Cytokinin signaling stabilizes the response activator ARR1. Plant 78(1):157–168. https://doi.org/10.1111/tpj.12458
Lei YB, Song SQ, Fu JR, Cheng HY (2004) Two-component signaling systems in plants. Chin Bullet Bot 21:216–227. https://doi.org/10.3969/j.issn.1674-3466.2004.02.012
Li R (2016) Oil palm: The pioneer of tropical agriculture going out. China Forestry Industry 10:63–64
Li JT, Fan HY, Zhao QQ, Lu DY, Yang YN, Yi QP, Liu MY, Jia YF, Peng B, Jian QM (2019) Research of abscisic acid modulated auxin biosynthesis and transport in rice root. J Xinyang Norm Uni (natural Science Edition) 32:39–46. https://doi.org/10.3969/j.issn.1003-0972.2019.01.007
Li XH, Wu M, Liu GY, Pei WF, Zhai HH, Yu JW, Zhang JF, Yu SX (2017) Identification of candidate genes for fiber length quantitative trait loci through RNA-Seq and linkage and physical mapping in cotton. BMC Genomics 18. https://doi.org/10.1186/s12864-017-3812-5
Li B, Huang J, Wang L, Li J, Liang YY, Chen J (2020) A review on how plant hormones and environment factors are involved in rice root hair development. Chin J Rice Sci 34:287–299. https://doi.org/10.16819/j.1001-7216.2020.9138
Li YY (2018) Oil palm (Elaeis guineensis jacq.) pollination biological characteristics and expression analysis of the related genes. Hainan University.
Liu XX, Zeng YZ, Li DD, Zheng YS (2020) Bioinformatics analysis of plant hormone-related genes in oil palm. Mol Plant Breed 18:3493–3501. https://doi.org/10.13271/j.mpb.018.003493
Liu ZN (2016) Study the regulation mechanism of plant two-component system on female gametophyte development and identification, evolution and expression analysis of the related gene families in Brassica rapa L. Zhejiang University.
Ljung K (2013) Auxin metabolism and homeostasis during plant development. Dev 140:943–950. https://doi.org/10.1242/dev.086363
Lord EM, Russell SD (2002) The mechanisms of pollination and fertilization in plants. Annu Rev Cell Dev Biol 18:81–105
Lu FZ, Wang KX, Yan LM, Peng YL, Qu JT, Wu J, Cao Y, Yang QQ, Fu FL, Yu HQ (2020) Isolation and characterization of maize ZmPP2C26 gene promoter in drought-response. Physiol Mol Bio Plants 26:2189–2197. https://doi.org/10.1007/s12298-020-00910-2
Lv JH, Pang QQ, Chen XQ, Li T, Fang JG, Lin SY, Jia HF (2020) Transcriptome analysis of strawberry fruit in response to exogenous arginine. Planta 252:82. https://doi.org/10.1007/s00425-020-03489-w
Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068. https://doi.org/10.1126/science.1172408
Ma KF, Song YP, Huang Z, Lin LY, Zhang ZY, Zhang DQ (2013) The low fertility of Chinese white poplar: dynamic changes in anatomical structure, endogenous hormone concentrations, and key gene expression in the reproduction of a naturally occurring hybrid. Plant Cell Rep 32:401–414. https://doi.org/10.1007/s00299-012-1373-2
Mano Y, Nemoto K (2012) The pathway of auxin biosynthesis in plants. J Exp Bot 63:2853–2872. https://doi.org/10.1093/jxb/ers091
McGaw BA, Horgan R (1983) Cytokinin catabolism and cytokinin oxidase. Phytochem 22:1103–1105. https://doi.org/10.1016/0031-9422(83)80200-3
Meng WJ (2018) Type-B Arabidopsis response regulators regulate regeneration and maintenance of shoot apical meristem. Shandong Agricultural Uni.
Mesejo C, Yuste R, Fuentes AM, Reig C, Iglesias DJ, Millo EP, Agustí M (2013) Self-pollination and parthenocarpic ability in developing ovaries of self-incompatible Clementine mandarins (Citrus clementina). Physiologia Plant 148:87–96. https://doi.org/10.1111/j.1399-3054.2012.01697.x
Niu YZ, Liao JG, Suo WL, Chen ZY, Pan ZH, Wei XM, Ma WG, Chen SY (2018) Research progress on the regulation mechanism of pollen-pistil interactions in Nicotiana. J Yunnan Univ Nat 40:1254–1260. https://doi.org/10.7540/j.ynu.20180239
Park SY, Fung P, Nishimura N et al (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of start proteins. Science 324:1068–1071. https://doi.org/10.1126/science.1173041
Peng H (2017) Function analysis of SlPYLs gene family of tomato. University of Chinese Academy of Sciences.
Qin ZW, Ren MJ, Zhou XY, Xin M (2017) Change of cucumber seed yield lines endogenous hormone during the process of double fertilization. J Northeast Agricul Uni 48:24–32. https://doi.org/10.3969/j.issn.1005-9369.2017.06.004
Qin YH, Zhang YZ, Bai PX, Wang LY, Cheng H, Wei K (2020) Identification and expression analysis of GH3 family gene in Camellia sinensis. Tea Comm 47:382–392
Rodrigues A, Adamo M, Crozet P, Margalha L, Confraria A, Martinho C, Elias A, Rabissi A, Lumbreras V, González-Guzmán M, Antoni R, Rodriguez PL, Baena-González E (2013) ABI1 and PP2CA phosphatases are negative regulators of Snf1-related protein kinase1 signaling in Arabidopsis. Plant Cell 25:3871–3884. https://doi.org/10.1105/TPC.113.114066
Sakai H, Honma T, Aoyama T, Sato S, Kato T, Tabata S, Oka A (2001) ARR1, a transcription factor for genes immediately responsive to cytokinins. Science 294:1519–1521. https://doi.org/10.1126/science.1065201
Santos MF, Johan M, Remko O (2009) Auxin-induced, SCFTIR1-mediated poly-ubiquitination marks AUX/IAA proteins for degradation. The Plant 59:100–109. https://doi.org/10.1111/j.1365-313X.2009.03854.x
Sato A, Sasaki S, Matsuzaki J, Yamamoto KT (2014) Light-dependent gravitropism and negative phototropism of inflorescence stems in a dominant Aux/IAA mutant of Arabidopsis thaliana, axr2. J Plant Res 127:627–639. https://doi.org/10.1007/s10265-014-0643-1
Schweighofer A, Hirt H, Meskiene I (2004) Plant PP2C phosphatases: emerging functions in stress signaling. Trends Plant Sci 9:236–243. https://doi.org/10.1016/j.tplants.2004.03.007
Shu K, Meng YJ, Shuai HW, Liu WG, Du JB, Liu J, Yang WY (2015) Dormancy and germination: How does the crop seed decide? Plant Biol 17:1104–1112. https://doi.org/10.1111/plb.12356
Singh R, Meilina OA, Leslie LET et al (2013) Oil palm genome sequence reveals divergence of interfertile species in Old and New worlds. Nature 500:335–339. https://doi.org/10.1038/nature12309
Somyong S, Walayaporn K, Jomchai N, Naktang C, Yodyingyong T, Phumichai C, Pootakham W, Tangphatsornruang S (2018) Transcriptome analysis of oil palm inflorescences revealed candidate genes for an auxin signaling pathway involved in parthenocarpy. PeerJ 6:e5975. https://doi.org/10.7717/peerj.5975
Song SQ, Liu J, Xu HH, Liu X, Huang H (2020) ABA metabolism and signaling and their molecular mechanism regulating seed dormancy and germination. Sci Agricult Sinica 53:857–873. https://doi.org/10.3864/j.issn.0578-1752.2020.05.001
Song S, Huang DM, Ma WH, Wang JS, Zhou ZX, Xu Y (2018) Auxin response factor (ARF) and plant genetic breeding. Mol Plant Breed 16:2638–2645. https://doi.org/10.13271/j.mpb.016.002638
Sowunmi MA (1999) The significance of the oil palm (Elaeis guineensis Jacq.) in the late Holocene environments of west and west central Africa: A further consideration. Veg Hist Archaeobot 8:199–210. https://doi.org/10.1007/BF02342720
Spartz AK, Lee SH, Wenger JP, Gonzalez N, Itoh H, Inzé D, Peer WA, Murphy AS, Overvoorde PJ, Gray WM (2012) The SAUR19 subfamily of SMALL AUXIN UP RNA genes promote cell expansion. The Plant 70:978–990. https://doi.org/10.1111/j.1365-313X.2012.04946.x
Tan X, Calderon-Villalobos LIA, Sharon M, Zheng CX, Robinson CV, Estelle M, Zheng N (2007) Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446:640–645. https://doi.org/10.1038/nature05731
Teh HF, Neoh BK, Wong YC, Kwong QB, Ooi TE, Ng TL et al (2014) Hormones, polyamines, and cell wall metabolism during oil palm fruit mesocarp development and ripening. J Agric Food Chem 62:8143–8152. https://doi.org/10.1021/jf500975h
Tranbarger TJ, Dussert S, Joët T, Argout X, Summo M, Champion A, Cros D, Omore A, Nouy B, Morcillo F (2011) Regulatory mechanisms underlying oil palm fruit mesocarp maturation, ripening, and functional specialization in lipid and carotenoid metabolism. Plant Physiol 156(2):564–584. https://doi.org/10.1104/pp.111.175141
Wang Y, Htwe YM, Ihase LO, Shi P, Cao HX, Lei XT (2018) Pollen germination genes differentially expressed in different pollens from Dura, Pisifera and Tenera oil palm (Elaeis guineensis jacq.). Sci Hort 235:32–38. https://doi.org/10.1016/j.scienta.2018.02.004
Wang XJ, Guo C, Peng J, Li C, Wan FF, Zhang SM, Zhou YY, Yan Y, Qi LJ, Sun KW, Yang SH, Gong ZZ, Li JG (2019) ABRE-BINDING FACTORS play a role in the feedback regulation of ABA signaling by mediating rapid ABA induction of ABA co-receptor genes. New Phytol 221:341–355. https://doi.org/10.1111/nph.15345
Wang GR, Yuan Z, Zhang PY, Qiu X, Liu ZX, Wang TC, Wei L (2020a) Expression and protein interactions analysis of ZmPP2C3 gene in maize (Zea mays). J Agricult Biotech 28:389–398. https://doi.org/10.3969/j.issn.1674-7968.2020.03.002
Wang L, Lee M, Ye BQ, Yue GH (2020b) Genes, pathways and networks responding to drought stress in oil palm roots. Sci Rep 10:21303. https://doi.org/10.1038/s41598-020-78297-z
Werner T, Köllmer I, Bartrina I, Holst K, Schmülling T (2006) New insights into the biology of cytokinin degradation. Plant Biol 8:371–381. https://doi.org/10.1055/s-2006-923928
Wong JH, Klejchová M, Snipes SA, Nagpal P, Bak G, Wang B, Dunlap S, Park MY, Kunkel EN, Trinidad B, Reed JW, Blatt MR, Gray WM (2020) SAUR proteins and PP2C.D phosphatases regulate H+-ATPases and K+ channels to control stomatal movements. Plant Physiol 185:256–273. https://doi.org/10.1093/PLPHYS/KIAA023
Wu JZ, Qin Y, Zhao J (2008) Pollen tube growth is affected by exogenous hormones and correlated with hormone changes in styles in Torenia fournieri L. Plant Growth Regul 55:137–148. https://doi.org/10.1007/s10725-008-9268-5
Xiong HB, Li R, Li XJ, Fan HK, Ma ZL (2009) Investigation, analysis and the advice of palm industry in China. Chin Agricult Sci Bullet 25:114–117
Yan ZY, Cao JJ, Fan QL, Chao HM, Guan XM, Zhang ZM, Duanmu DQ (2020) Dephosphorylation of LjMPK6 by phosphatase LjPP2C is involved in regulating nodule organogenesis in Lotus japonicus. Int J Mol Sci 21:5565. https://doi.org/10.3390/ijms21155565
Yang XL, Yang LP, Shang AQ, Liu FL (2009) Relationship between protective enzymes, endogenous hormones in pistil and pollination compatibility of lilium. Acta Hort Sinica 36:855–860. https://doi.org/10.3321/j.issn:0513-353X.2009.06.012
Yasushi T, Tomomi S, Takafumi Y, Takeshi M (2004) Comparative studies of the AHP histidine-containing phosphotransmitters implicated in His-to-Asp phosphorelay in Arabidopsis thaliana. Biosci Biotech Biochem 68:462–465. https://doi.org/10.1271/BBB.68.462
Zenser N, Ellsmore A, Leasure C, Callis J (2001) Auxin modulates the degradation rate of Aux/IAA proteins. Proc Nat Acad Sci 98:11795–11800. https://doi.org/10.1073/pnas.211312798
Zhao TT, Ren LJ, Chen XJ, Yu HX, Liu CJ, Shen Y, Shi WQ, Tang D, Du GJ, Li YF, Ma BJ, Cheng ZK (2018) The OsRR24/LEPTO1 type-B response regulator is essential for the organization of leptotene chromosomes in rice meiosis. Plant Cell 30:3024–3037. https://doi.org/10.1105/TPC.18.00479
Acknowledgements
We would like to express our gratitude to MetWare Biotechnology Co., Ltd. (Wuhan, China) for transcriptome sequencing assistance. This research was supported by Central Public-interest Scientific Institution Basal Research Fund for the Chinese Academy of Tropical Agricultural Sciences (No.1630052021028 and No. 17CXTD-13).
Funding
This research was supported by Central Public-interest Scientific Institution Basal Research Fund for Chinese Academy of Tropical Agricultural Sciences (No. 1630052021028 and No. 17CXTD-13).
Author information
Authors and Affiliations
Contributions
MDY and RNZ designed and conducted the experiment, completed data analysis, and prepared the manuscript. YR and JJJM revised and corrected the manuscript. LFJ and LXZ participated in the experimental design and result analysis. HXC conceived the whole project, guided experimental design, data analysis, and manuscript writing. All authors have read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Key message
Transcriptomic study revealed the role of phytohormone biosynthesis and signaling genes during the pollination and fertilization of oil palm plants
Rights and permissions
About this article
Cite this article
Yang, M., Yarra, R., Zhang, R. et al. Transcriptome analysis of oil palm pistil during pollination and fertilization to unravel the role of phytohormone biosynthesis and signaling genes. Funct Integr Genomics 22, 261–278 (2022). https://doi.org/10.1007/s10142-022-00834-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10142-022-00834-y