Alteration of TAC1 expression in Prunus species leads to pleiotropic shoot phenotypes

Abstract

Prunus persica (peach) trees carrying the “Pillar” or “Broomy” trait (br) have vertically oriented branches caused by loss-of-function mutations in a gene called TILLER ANGLE CONTROL 1 (TAC1). TAC1 encodes a protein in the IGT gene family that includes LAZY1 and DEEPER ROOTING 1 (DRO1), which regulate lateral branch and root orientations, respectively. Here we found that some of the native TAC1 alleles in the hexaploid plum species Prunus domestica, which has a naturally more upright stature, contained a variable length trinucleotide repeat within the same exon 3 region previously found to be disrupted in pillar peach trees. RNAi silencing of TAC1 in plum resulted in trees with severely vertical branch orientations similar to those in pillar peaches but with an even narrower profile. In contrast, PpeTAC1 overexpression in plum led to trees with wider branch angles and more horizontal branch orientations. Pillar peach trees and transgenic plum lines exhibited pleiotropic phenotypes, including differences in trunk and branch diameter, stem growth, and twisting branch phenotypes. Expression profiling of pillar peach trees revealed differential expression of numerous genes associated with biotic and abiotic stress, hormone responses, plastids, reactive oxygen, secondary, and cell wall metabolism. Collectively, the data provide important clues for understanding TAC1 function and show that alteration of TAC1 expression may have broad applicability to agricultural and ornamental tree industries.

Opposing influences of TAC1 and LAZY1 on Lateral Shoot Orientation in Arabidopsis

“…6E, Supplementary Data File D4). A similar enrichment was reported for tac1 (pillar) peaches 17 . Supporting the known connection between LAZY1 and auxin transport, and in accordance with the lazy1 mutant phenotype, t0 lazy1 transcriptomes (when compared to t0 Col) were enriched for DEGs associated with hormone metabolism, the cell wall, and photosynthesis, among other categories ( Fig.…”

“…Ectopic LAZY1 expression causes an EAR-domain dependent curled leaf phenotype. We previously reported that overexpression of TAC1 in plum trees resulted in wider branch angles 17 . However, we also reported TAC1 overexpression only partially complemented the tac1 Arabidopsis mutant phenotype, and in 24-hour light or dark conditions TAC1 overexpression in Col had little effect on branch angle 3,18 .…”

“…However, species-wide interpretations of results from maize should be cautioned because in addition to its role in gravitropism and shoot architecture, LAZY1 is also essential for tassel and ear development in maize 5 .In contrast to the mechanistic knowledge about LAZY1, much less is known about TAC1. Its function in promoting wide lateral shoot angles is dosage dependent and light regulated 3,[13][14][15][16][17][18][19][32][33][34] . TAC1 expression has been detected in shoot tissues in peach, poplar, and Arabidopsis, with higher expression detected in apical regions 3,16,34 .…”

“…Arabidopsis 13,16,17 . 35 S::TAC1 lines were only minimally wider than Col while 35 S::LAZY1 also exhibited slightly wider branch angles, a strong contrast to previously reported narrow branch angle phenotype of 35 S::LAZY4/ DRO1 Arabidopsis 6 .…”

Manipulation of Growth and Architectural Characteristics in Trees for Increased Woody Biomass Production

“…TAC1 belongs to a small family of genes. All the genes in the family, characterized to date in several plant species, including trees (poplar and plum) control branch or lateral root angles ( Figure 1 ; Xu et al, 2017 ; Hollender et al, 2018 ). Depending on presence of a conserved domain, members of the family can increase ( TAC1 ) or decrease ( LAZY1 ) branch angles ( Figure 1 ; Dardick et al, 2013 ; Hollender and Dardick, 2015 ; Xu et al, 2017 ).…”