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

Abstract

(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 upregulated specifically by P starvation in an accessible tissue upstream of a marker gene such as ␤-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the expression of only four genes differed between shoots of P-starved and -replete plants 28 h after P was withdrawn.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.

Stress Response Versus Stress Tolerance: A Transcriptome Analysis of Two Rice Lines Contrasting in Tolerance to Phosphorus Deficiency

“…Plant response to P deficiency has been analyzed at the transcriptome level in both Arabidopsis (Hammond et al 2003;Misson et al 2005;Morcuende et al 2007) and rice (Wasaki et al 2003(Wasaki et al , 2006Wang et al 2006). These studies were carried out in nutrient solutions or other artificial media and had detected a series of adaptive responses at the transcriptome levels that (1) circumvent metabolic steps requiring Pi by utilizing alternative glycolytic or respiratory pathways; (2) alter the lipid composition by enzymatic degradation of phospholipids and synthesis of galactolipid and sulfolipids; (3) remobilize Pi through enhanced expression of phosphatases and RNases; (4) enhance Pi uptake and retranslocation via an upregulation of highaffinity Pi transporters; (5) alter the carbon skeleton flow with potential benefits for root growth or organic acid synthesis and exudation; and (6) are involved in signal transduction and transcriptional regulation.…”

“…Microarray studies in Arabidopsis thaliana (Hammond et al 2003;Misson et al 2005;Morcuende et al 2007) and rice (Wasaki et al 2003;Wang et al 2006;Wasaki et al 2006) have confirmed the Pi responsiveness of many gene families involved in Pi acquisition and P remobilization and redistribution. Despite the valuable insights gained from these studies, it has so far been difficult to draw practically relevant conclusions because distinguishing stress response mechanisms/genes from those leading to elevated tolerance remains difficult.…”

Promoter Analysis of the Barley Pht1;1 Phosphate Transporter Gene Identifies Regions Controlling Root Expression and Responsiveness to Phosphate Deprivation

“…However, P1BS-like elements are also present in multiple copies within the ubiquitin promoter, a promoter which does not respond to P deficiency (Schü nmann et al, 2004), and few cis elements have been shown to be functional in both monocots and dicots. Furthermore, even in Arabidopsis, the element was identified in the promoter regions of 15% to 20% of all genes and was not preferentially in promoters of P-regulated genes (Hammond et al, 2003). There is therefore, to date, no direct functional evidence that P1BS-like elements are associated with P-regulated expression of the Pi transporter genes, and the presence of the motif in itself is insufficient evidence to conclude a role in P regulation.…”

The Phosphate Fast-Responsive Genes PECP1 and PPsPase1 Affect Phosphocholine and Phosphoethanolamine Content

“…Most phosphorus in the soil is not available to plants, as it is combined with other minerals or parts of organic compounds (Bieleski, 1973;Raghothama and Karthikeyan, 2005). Only a small fraction of soluble Pi (usually present at a concentration of ,10 mM in the soil) can be taken up by plants.Although growth is not optimal under limiting conditions, plants can withstand changing Pi concentrations within heterogeneous soils or in the external nutrient supply that can lead to reprogramming of their metabolism and architecture (Hammond et al, 2003;Péret et al, 2011;Plaxton and Tran, 2011). Root architecture can be modified to facilitate Pi uptake by favoring the development of lateral roots (at the expense of primary root elongation in many plants including Arabidopsis), increasing the density and length of root hairs, and limiting the development of aerial parts (López-Bucio et al, 2002;Svistoonoff et al, 2007;Gruber et al, 2013).…”