Promotion of shoot development and tuberisation in potato by expression of a chimaeric cytokinin synthesis gene at normal and elevated CO2 levels
Guo-Qing Tao A D , D. Stuart Letham A , Jean W. H. Yong B E F , Kerong Zhang A C , Peter C. L. John A , Owen Schwartz A , S. Chin Wong B and Graham D. Farquhar BA Plant Cell Biology, Research School of Biology, Australian National University, PO Box 475, Canberra, ACT 2601, Australia.
B Environmental Biology, Research School of Biology, Australian National University, PO Box 475, Canberra, ACT 2601, Australia.
C Genomic Interactions, Research School of Biology, Australian National University, PO Box 475, Canberra, ACT 2601, Australia.
D Victoria Department of Primary Industries, Bundoora, Vic. 3083, Australia.
E Natural Sciences and Science Education Academic Group, National Institute of Education, Nanyang Technological University, Singapore.
F Corresponding author. Email: jean.yong@nie.edu.sg
Functional Plant Biology 37(1) 43-54 https://doi.org/10.1071/FP07032
Submitted: 3 February 2007 Accepted: 25 September 2009 Published: 5 January 2010
Abstract
The bacterial cytokinin biosynthesis gene ipt under control of a chalcone synthase promoter (PCHS) was introduced into potato (Solanum tuberosum L.). Two transgenic lines were selected for detailed study, because in these, root development was reduced only moderately, thus, enabling the plants to be grown in pots. Expression of the PCHS-ipt gene elevated the level of zeatin cytokinins markedly in the apical bud, subapical stems and leaves. The transgenic (IPT) plants exhibited a lower and denser leaf canopy relative to wild-type (WT) plants owing to reduction in main stem length, increase in node number per stem and promotion of lateral shoot development. Main stem diameter was increased markedly due to promotion of cell division associated with activation of cyclin-dependent kinase in the subapical stem. Expression of the PCHS-ipt gene induced aerial stolons, promoted growth of underground stolons and increased tuber number but reduced tuber weight and nitrogen content. The gene expression also increased pinnae and pinnule number per leaf, increased thickness of pinnae and promoted transpiration, photosynthesis and stomatal conductance – effects monitored by gas exchange and 18O and 13C analysis. The elevation of [CO2] to 900 μmol mol–1 promoted growth of both WT and IPT plants, ameliorated the negative effect of high cytokinin on tuber weight and interacted additively with ipt gene expression to promote stem growth.
Additional keywords: cyclin-dependent kinase, photosynthesis, stable isotopes.
Acknowledgements
The authors wish to thank Mr DA Willcocks for assistance in growing potato plants, Ms Jan Elliott for valuable help in preparing the manuscript.
Badenoch-Jones J,
Parker CW,
Letham DS, Singh S
(1996) Effect of cytokinins supplied via the xylem at multiples of endogenous concentrations on transpiration and senescence in derooted seedlings of oat and wheat. Plant, Cell & Environment 19, 504–516.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Champagne C, Sinha N
(2004) Compound leaves: equal to the sum of their parts. Development 131, 4401–4412.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
DeMason DA
(2005) Auxin–cytokinin and auxin–gibberellin interactions during morphogenesis of the compound leaves of pea. Planta 222, 151–166.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Faiss M,
Zalubilova Z,
Strnad M, Schmülling T
(1997) Conditional transgenic expression of the ipt gene indicates a function for cytokinins in paracrine signalling in whole tobacco plants. The Plant Journal 12, 401–415.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Farquhar GD,
Ehleringer JR, Hubick KT
(1989) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology 40, 503–537.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Farquhar GD,
Henry BK, Styles JM
(1997) A rapid on-line technique for determination of oxygen isotope composition of nitrogen-containing organic matter and water. Rapid Communications in Mass Spectrometry 11, 1554–1560.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Gális I,
Macas J,
Vlasák J,
Ondřej M, Van Onckelen HA
(1995) The effect of an elevated cytokinin level using the ipt gene and N6-benzyl-adenine on single node and intact potato plant tuberization. Journal of Plant Growth Regulation 14, 143–150.
| Crossref | GoogleScholarGoogle Scholar |
Gan S, Amasino RM
(1995) Inhibition of leaf senescence by autoregulated production on cytokinin. Science 270, 1986–1988.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Hepler PK,
Sek FJ, John PCL
(1994) Nuclear concentration and mitotic dispersion of the essential cell cycle protein p13suc1 examined in living cells. Proceedings of the National Academy of Sciences of the United States of America 91, 2176–2180.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
John PCL,
Sek FJ, Hayles J
(1991) Association of the plant p34cdc2-like protein with p13suc1: implications for control of cell division cycles in plants. Protoplasma 161, 70–74.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Jordi W,
Schapendonk A,
Davelaar E,
Stoopen GM,
Pot CS,
De Visser R,
Van Rhijn JA,
Gan S, Amasino RM
(2000) Increased cytokinin levels in transgenic PSAG12-IPT tobacco plants have large direct and indirect effects on leaf senescence, photosynthesis and N partitioning. Plant, Cell & Environment 23, 279–289.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Joubès J,
Chevalier C,
Dudits D,
Heberle-Bors E,
Inzé D,
Umeda M, Renaudin JP
(2000) CDK-related protein kinases in plants. Plant Molecular Biology 43, 607–620.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Li Y,
Hagen G, Guilfoyle TJ
(1992) Altered morphology in transgenic tobacco plants that overproduce cytokinins in specific tissue and organs. Developmental Biology 153, 386–395.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ma QH
(2008) Genetic engineering of cytokinins and their applications to agriculture. Critical Reviews in Biotechnology 28, 213–232.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
McBride KE, Summerfelt KR
(1990) Improved binary vectors for Agrobacterium-mediated plant transformation. Plant Molecular Biology 14, 269–276.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
McKenzie MJ,
Mett V,
Reynolds PHS, Jameson PE
(1998) Controlled cytokinin production in transgenic tobacco using a copper-inducible promoter. Plant Physiology 116, 969–977.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Miyawaki K,
Matsumoto-Kitano M, Kakimoto T
(2004) Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin and nitrate. The Plant Journal 37, 128–138.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Miyawaki K,
Tarkowski P,
Matsumoto-Kitano M,
Kato T,
Sato S,
Tarkowska D,
Tabata S,
Sandberg G, Kakimoto T
(2006) Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferase in cytokinin biosynthesis. Proceedings of the National Academy of Sciences of the United States of America 103, 16 598–16 603.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Moran R, Porath D
(1980) Chlorophyll determination in intact tisues using N,N-dimethyl-formamide. Plant Physiology 65, 478–479.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Murashige T, Skoog F
(1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum 15, 473–497.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Nurse P
(1990) Universal control mechanism regulatory onset of M-phase. Nature 344, 503–508.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ooms G, Lenton JR
(1985) T-DNA genes to study plant development: precocious tuberization and enhanced cytokinins in A. tumerfaciens transformed potato. Plant Molecular Biology 5, 205–212.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Ooms G,
Risiott R,
Kendall A,
Keys A,
Lawlor D,
Smith S,
Turner J, Young A
(1991) Phenotypic changes in T-cyt-transformed potato plants are consistent with enhanced sensitivity of specific cell types to normal regulation by root-derived cytokinin. Plant Molecular Biology 17, 727–743.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Parker CW,
Badenoch-Jones J, Letham DS
(1989) Radioimmunoassay for quantifying the cytokinins cis-zeatin and cis-zeatin riboside and its application to xylem sap samples. Journal of Plant Growth Regulation 8, 93–105.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Peters W,
Füchtbauer B, Beck E
(1995) Nitrate reductase activity is endogenously induced by zeatin riboside in habituated suspension cultured Chenopodium rubrum cells. Journal of Plant Physiology 147, 401–407.
|
CAS |
Riou-Khamlichi C,
Huntley R,
Jacqmard A, Murray JAH
(1999) Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283, 1541–1544.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Rosin FM,
Hart JK,
Van Onckelen H, Hannapel DJ
(2003) Suppression of a vegetative MADS box gene of potato activates axillary meristem development. Plant Physiology 131, 1613–1622.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Sergeeva LI,
de Bruijn SM,
Koot-Gronsveld EAM,
Navratil O, Vreugdenhil D
(2000) Tuber morphology and starch accumulation are independent phenomena: evidence from ipt-transgenic potato lines. Physiologia Plantarum 108, 435–443.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Sicher RC, Bunce JA
(1999) Photosynthetic enhancement and conductance to water vapor of field-grown Solanum tuberosum (L.) in response to CO2 enrichment. Photosynthesis Research 62, 155–163.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Singh S,
Letham DS,
Jameson PE,
Zhang R,
Parker CW,
Badenoch-Jones J, Noodén LD
(1988) Cytokinin biochemistry in relation to leaf senescence. IV. Cytokinin metabolism in soybean explants. Plant Physiology 88, 788–794.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Synková H,
Van Loven K,
Pospíšilová J, Valcke RLM
(1999) Photosynthesis of transgenic Pssu-ipt tobacco. Journal of Plant Physiology 155, 173–182.
Trippi VS, Palacios LR
(1970) Leaf shape induced by the cytokinins kinetin and benzyladenine in Phaseolus vulgaris. Phyton 27, 7–10.
|
CAS |
Van Loven K,
Beinsberger SEL,
Valcke RLM,
Van Onckelen HA, Clijsters HMM
(1993) Morphometric analysis of the growth of Phsp70-ipt transgenic tobacco plants. Journal of Experimental Botany 44, 1671–1678.
| Crossref | GoogleScholarGoogle Scholar |
Wang J,
Letham DS,
Taverner E,
Badenoch-Jones J, Hocart CH
(1995) A procedure for quantification of cytokinins as free bases involving scintillation proximity immunoassay. Physiologia Plantarum 95, 91–98.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Wang J,
Letham DS,
Cornish E, Stevenson KR
(1997a) Studies of cytokinin action and metabolism using tobacco plants expressing either the ipt or the GUS gene controlled by a chalcone synthase promoter. I. Developmental features of the transgenic plants. Australian Journal of Plant Physiology 24, 661–672.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Wang J,
Letham DS,
Cornish E,
Wei I,
Hocart CH,
Michael M, Stevenson KR
(1997b) Studies of cytokinin action and metabolism using tobacco plants expressing either the ipt or the GUS gene controlled by a chalcone synthase promoter II. ipt and GUS gene expression, cytokinin levels and metabolism. Australian Journal of Plant Physiology 24, 673–683.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Werner T,
Holst K,
Pors Y,
Guivarch A,
Mustroph A,
Chriqui D,
Grimm B, Schmulling T
(2008) Cytokinin deficiency causes distinct changes of sink and source parameters in tobacco shoots and roots. Journal of Experimental Botany 59, 2659–2672.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Yong JWH,
Wong SC, Farquhar GD
(1997) Stomatal responses to changes in vapour pressure difference between leaf and air. Plant, Cell & Environment 20, 1213–1216.
| Crossref | GoogleScholarGoogle Scholar |
Yong JWH,
Wong SC,
Letham DS,
Hocart CH, Farquhar GD
(2000) Effects of elevated [CO2] and nitrogen nutrition on cytokinins in the xylem sap and leaves of cotton. Plant Physiology 124, 767–780.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Zhang K,
Letham DS, John PCL
(1996) Cytokinin controls the cell cycle at mitosis by stimulating the tyrosine dephosphorylation and activation of p34cdc2-like Hi histone kinase. Planta 200, 2–12.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Zhang K,
Diederich L, John PCL
(2005) The cytokinin requirement for cell division in cultured Nicotiana plumbaginifolia cells can be satisfied by yeast cdc25 protein tyrosine phosphatase. Implications for mechanisms of cytokinin response and plant development. Plant Physiology 137, 308–316.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Zubko E,
Macháčková I,
Malbck J, Meyer P
(2005) Modification of cytokinin level in potato via expression of the Petunia hybrida Sho gene is regulated by auxin in transgenic tobacco tissues. Transgenic Research 14, 615–618.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
