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First published online May 15, 2003; 10.1104/pp.103.020941

Plant Physiology 132:578-596 (2003)
© 2003 American Society of Plant Biologists

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RESEARCH PAPERS ON SYSTEMS BIOLOGY/GENOMICS/BIOINFORMATICS

Changes in Gene Expression in Arabidopsis Shoots during Phosphate Starvation and the Potential for Developing Smart Plants1

John P. Hammond, Malcolm J. Bennett, Helen C. Bowen, Martin R. Broadley, Dan C. Eastwood, Sean T. May, Clive Rahn, Ranjan Swarup, Kathryn E. Woolaway and Philip J. White*

Horticulture Research International, Wellesbourne, Warwick CV35 9EF, United Kingdom (J.P.H., H.C.B., M.R.B., D.C.E., C.R., K.E.W., P.J.W.); and Plant Science Division, Nottingham University, Sutton Bonington Campus, Loughborough LE12 5RD, United Kingdom (J.P.H., M.J.B., S.T.M., R.S.)

Our aim was to generate and prove the concept of "smart" plants to monitor plant phosphorus (P) status in Arabidopsis. Smart plants can be genetically engineered by transformation with a construct containing the promoter of a gene up-regulated specifically by P starvation in an accessible tissue upstream of a marker gene such as {beta}-glucuronidase (GUS). First, using microarrays, we identified genes whose expression changed more than 2.5-fold in shoots of plants growing hydroponically when P, but not N or K, was withheld from the nutrient solution. The transient changes in gene expression occurring immediately (4 h) after P withdrawal were highly variable, and many nonspecific, shock-induced genes were up-regulated during this period. However, two common putative cis-regulatory elements (a PHO-like element and a TATA box-like element) were present significantly more often in the promoters of genes whose expression increased 4 h after the withdrawal of P compared with their general occurrence in the promoters of all genes represented on the microarray. Surprisingly, the expression of only four genes differed between shoots of P-starved and -replete plants 28 h after P was withdrawn. This lull in differential gene expression preceded the differential expression of a new group of 61 genes 100 h after withdrawing P. A literature survey indicated that the expression of many of these "late" genes responded specifically to P starvation. Shoots had reduced P after 100 h, but growth was unaffected. The expression of SQD1, a gene involved in the synthesis of sulfolipids, responded specifically to P starvation and was increased 100 h after withdrawing P. Leaves of Arabidopsis bearing a SQD1::GUS construct showed increased GUS activity after P withdrawal, which was detectable before P starvation limited growth. Hence, smart plants can monitor plant P status. Transferring this technology to crops would allow precision management of P fertilization, thereby maintaining yields while reducing costs, conserving natural resources, and preventing pollution.

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.020941.

1 This work was supported by the Biotechnology and Biological Sciences Research Council (UK), by the Department for Environment, Food and Rural Affairs (UK; project nos. HH0915SFV, HH3502SFV, and HH3501SFV), and by a Horticulture Research International Gordon Browning Studentship to J.P.H.

* Corresponding author; e-mail philip-j.white{at}hri.ac.uk; fax 01789–470552.

Received January 24, 2003; returned for revision February 28, 2003; accepted March 9, 2003.




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